Regulation of vascular integrity

Journal of Molecular Medicine

Volumn 87, Issue 6, 2009, Pages 571-582

  Murakami, Masahiro ^a   Simons, Michael ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cadherin; Endothelial junction; Extracellular matrix; Integrin; Pericyte; Permeability; Vascular integrity

Indexed keywords

BLEEDING; BLOOD VESSEL PERMEABILITY; CELL JUNCTION; CELL MEMBRANE PERMEABILITY; EDEMA; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; INFLAMMATION; ISCHEMIA; KNOCKOUT MOUSE; NONHUMAN; PERICYTE; REVIEW;

ANIMALS; BLOOD VESSELS; ENDOTHELIUM, VASCULAR; EXTRACELLULAR MATRIX; HEMODYNAMICS; HUMANS; MODELS, BIOLOGICAL; NEOVASCULARIZATION, PHYSIOLOGIC; PERICYTES;

EID: 67349220264     PISSN: 09462716     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00109-009-0463-2     Document Type: Review

References (112)

1. P Carmeliet 2005 Angiogenesis in life, disease and medicine Nature 438 932 936 (Pubitemid 43093958)
2. M Simons 2005 Angiogenesis: where do we stand now? Circulation 111 1556 1566 (Pubitemid 40470653)
3. RK Jain 2005 Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy Science 307 58 62 (Pubitemid 40093472)
4. C Stockmann A Doedens A Weidemann N Zhang N Takeda JI Greenberg DA Cheresh RS Johnson 2008 Deletion of vascular endothelial growth factor in myeloid cells accelerates tumorigenesis Nature 456 814 818
5. U Fiedler HG Augustin 2006 Angiopoietins: a link between angiogenesis and inflammation Trends Immunol 27 552 558 (Pubitemid 44780853)
6. M Murakami M Simons 2008 Fibroblast growth factor regulation of neovascularization Curr Opin Hematol 15 215 220
7. MS Pepper 1997 Transforming growth factor-beta: vasculogenesis, angiogenesis, and vessel wall integrity Cytokine Growth Factor Rev 8 21 43 (Pubitemid 27214687)
8. C Betsholtz 2004 Insight into the physiological functions of PDGF through genetic studies in mice Cytokine Growth Factor Rev 15 215 228 (Pubitemid 38781047)
9. J Andrae R Gallini C Betsholtz 2008 Role of platelet-derived growth factors in physiology and medicine Genes Dev 22 1276 1312
10. RO Hynes 2007 Cell-matrix adhesion in vascular development J Thromb Haemost 5 Suppl 1 32 40 (Pubitemid 46964284)
11. N Simionescu M Simionescu GE Palade 1978 Open junctions in the endothelium of the postcapillary venules of the diaphragm J Cell Biol 79 27 44 (Pubitemid 9035436)
12. NK Tonks 2006 Protein tyrosine phosphatases: from genes, to function, to disease Nat Rev Mol Cell Biol 7 833 846 (Pubitemid 44627477)
13. E Dejana 2004 Endothelial cell-cell junctions: happy together Nat Rev Mol Cell Biol 5 261 270 (Pubitemid 38480607)
14. A Taddei C Giampietro A Conti F Orsenigo F Breviario V Pirazzoli M Potente C Daly S Dimmeler E Dejana 2008 Endothelial adherens junctions control tight junctions by VE-cadherin-mediated upregulation of claudin-5 Nat Cell Biol 10 923 934
15. S Yamada S Pokutta F Drees WI Weis WJ Nelson 2005 Deconstructing the cadherin-catenin-actin complex Cell 123 889 901 (Pubitemid 41721034)
16. SM Weis DA Cheresh 2005 Pathophysiological consequences of VEGF-induced vascular permeability Nature 437 497 504 (Pubitemid 41613541)
17. MD Potter S Barbero DA Cheresh 2005 Tyrosine phosphorylation of VE-cadherin prevents binding of p120- and beta-catenin and maintains the cellular mesenchymal state J Biol Chem 280 31906 31912 (Pubitemid 41291941)
18. Y Wallez F Cand F Cruzalegui C Wernstedt S Souchelnytskyi I Vilgrain P Huber 2007 Src kinase phosphorylates vascular endothelial-cadherin in response to vascular endothelial growth factor: identification of tyrosine 685 as the unique target site Oncogene 26 1067 1077 (Pubitemid 46272205)
19. U Baumeister R Funke K Ebnet H Vorschmitt S Koch D Vestweber 2005 Association of Csk to VE-cadherin and inhibition of cell proliferation Embo J 24 1686 1695 (Pubitemid 40704979)
20. J Gavard JS Gutkind 2006 VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin Nat Cell Biol 8 1223 1234 (Pubitemid 44660587)
21. P Carmeliet MG Lampugnani L Moons F Breviario V Compernolle F Bono G Balconi R Spagnuolo B Oostuyse M Dewerchin A Zanetti A Angellilo V Mattot D Nuyens E Lutgens F Clotman MC de Ruiter A Gittenberger-de Groot R Poelmann F Lupu JM Herbert D Collen E Dejana 1999 Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis Cell 98 147 157 (Pubitemid 29344903)
22. A Cattelino S Liebner R Gallini A Zanetti G Balconi A Corsi P Bianco H Wolburg R Moore B Oreda R Kemler E Dejana 2003 The conditional inactivation of the beta-catenin gene in endothelial cells causes a defective vascular pattern and increased vascular fragility J Cell Biol 162 1111 1122 (Pubitemid 37174193)
23. R Nawroth G Poell A Ranft S Kloep U Samulowitz G Fachinger M Golding DT Shima U Deutsch D Vestweber 2002 VE-PTP and VE-cadherin ectodomains interact to facilitate regulation of phosphorylation and cell contacts Embo J 21 4885 4895
24. S Baumer L Keller A Holtmann R Funke B August A Gamp H Wolburg K Wolburg-Buchholz U Deutsch D Vestweber 2006 Vascular endothelial cell-specific phosphotyrosine phosphatase (VE-PTP) activity is required for blood vessel development Blood 107 4754 4762 (Pubitemid 43882626)
25. AF Nottebaum G Cagna M Winderlich AC Gamp R Linnepe C Polaschegg K Filippova R Lyck B Engelhardt O Kamenyeva MG Bixel S Butz D Vestweber 2008 VE-PTP maintains the endothelial barrier via plakoglobin and becomes dissociated from VE-cadherin by leukocytes and by VEGF J Exp Med 205 2929 2945
26. M Corada M Mariotti G Thurston K Smith R Kunkel M Brockhaus MG Lampugnani I Martin-Padura A Stoppacciaro L Ruco DM McDonald PA Ward E Dejana 1999 Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo Proc Natl Acad Sci U S A 96 9815 9820 (Pubitemid 29398815)
27. M Corada L Zanetta F Orsenigo F Breviario MG Lampugnani S Bernasconi F Liao DJ Hicklin P Bohlen E Dejana 2002 A monoclonal antibody to vascular endothelial-cadherin inhibits tumor angiogenesis without side effects on endothelial permeability Blood 100 905 911 (Pubitemid 34832616)
28. F Liao Y Li W O'Connor L Zanetta R Bassi A Santiago J Overholser A Hooper P Mignatti E Dejana DJ Hicklin P Bohlen 2000 Monoclonal antibody to vascular endothelial-cadherin is a potent inhibitor of angiogenesis, tumor growth, and metastasis Cancer Res 60 6805 6810 (Pubitemid 32059142)
29. L Zanetta M Corada M Grazia Lampugnani A Zanetti F Breviario L Moons P Carmeliet MS Pepper E Dejana 2005 Downregulation of vascular endothelial-cadherin expression is associated with an increase in vascular tumor growth and hemorrhagic complications Thromb Haemost 93 1041 1046 (Pubitemid 40823506)
30. R Cao A Eriksson H Kubo K Alitalo Y Cao J Thyberg 2004 Comparative evaluation of FGF-2-, VEGF-A-, and VEGF-C-induced angiogenesis, lymphangiogenesis, vascular fenestrations, and permeability Circ Res 94 664 670 (Pubitemid 38387750)
31. M Murakami LT Nguyen ZW Zhang KL Moodie P Carmeliet RV Stan M Simons 2008 The FGF system has a key role in regulating vascular integrity J Clin Invest 118 3355 3366
32. M Grazia Lampugnani A Zanetti M Corada T Takahashi G Balconi F Breviario F Orsenigo A Cattelino R Kemler TO Daniel E Dejana 2003 Contact inhibition of VEGF-induced proliferation requires vascular endothelial cadherin, beta-catenin, and the phosphatase DEP-1/CD148 J Cell Biol 161 793 804 (Pubitemid 36648762)
33. C Suri PF Jones S Patan S Bartunkova PC Maisonpierre S Davis TN Sato GD Yancopoulos 1996 Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis Cell 87 1171 1180 (Pubitemid 27010101)
34. DJ Dumont G Gradwohl GH Fong MC Puri M Gertsenstein A Auerbach ML Breitman 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 (Pubitemid 24273890)
35. TN Sato Y Tozawa U Deutsch K Wolburg-Buchholz Y Fujiwara M Gendron-Maguire T Gridley H Wolburg W Risau Y Qin 1995 Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation Nature 376 70 74
36. J Gavard V Patel JS Gutkind 2008 Angiopoietin-1 prevents VEGF-induced endothelial permeability by sequestering Src through mDia Dev Cell 14 25 36
37. S Fukuhara K Sako T Minami K Noda HZ Kim T Kodama M Shibuya N Takakura GY Koh N Mochizuki 2008 Differential function of Tie2 at cell-cell contacts and cell-substratum contacts regulated by angiopoietin-1 Nat Cell Biol 10 513 526
38. P Saharinen L Eklund J Miettinen R Wirkkala A Anisimov M Winderlich A Nottebaum D Vestweber U Deutsch GY Koh BR Olsen K Alitalo 2008 Angiopoietins assemble distinct Tie2 signalling complexes in endothelial cell-cell and cell-matrix contacts Nat Cell Biol 10 527 537
39. A Armulik A Abramsson C Betsholtz 2005 Endothelial/pericyte interactions Circ Res 97 512 523 (Pubitemid 41361741)
40. H Gerhardt H Semb 2008 Pericytes: gatekeepers in tumour cell metastasis? J Mol Med 86 135 144
41. G Bergers S Song 2005 The role of pericytes in blood-vessel formation and maintenance Neuro Oncol 7 452 464 (Pubitemid 41555617)
42. A Antonelli-Orlidge KB Saunders SR Smith PA D'Amore 1989 An activated form of transforming growth factor beta is produced by cocultures of endothelial cells and pericytes Proc Natl Acad Sci U S A 86 4544 4548 (Pubitemid 19164588)
43. Y Sato DB Rifkin 1989 Inhibition of endothelial cell movement by pericytes and smooth muscle cells: activation of a latent transforming growth factor-beta 1-like molecule by plasmin during co-culture J Cell Biol 109 309 315 (Pubitemid 19180138)
44. SJ Mandriota PA Menoud MS Pepper 1996 Transforming growth factor beta 1 down-regulates vascular endothelial growth factor receptor 2/flk-1 expression in vascular endothelial cells J Biol Chem 271 11500 11505 (Pubitemid 26155993)
45. KK Hirschi SA Rohovsky PA D'Amore 1998 PDGF, TGF-beta, and heterotypic cell-cell interactions mediate endothelial cell-induced recruitment of 10 T1/2 cells and their differentiation to a smooth muscle fate J Cell Biol 141 805 814 (Pubitemid 28217923)
46. MC Dickson JS Martin FM Cousins AB Kulkarni S Karlsson RJ Akhurst 1995 Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice Development 121 1845 1854
47. M Oshima H Oshima MM Taketo 1996 TGF-beta receptor type II deficiency results in defects of yolk sac hematopoiesis and vasculogenesis Dev Biol 179 297 302 (Pubitemid 26363265)
48. DY Li LK Sorensen BS Brooke LD Urness EC Davis DG Taylor BB Boak DP Wendel 1999 Defective angiogenesis in mice lacking endoglin Science 284 1534 1537
49. LD Urness LK Sorensen DY Li 2000 Arteriovenous malformations in mice lacking activin receptor-like kinase-1 Nat Genet 26 328 331
50. SP Oh T Seki KA Goss T Imamura Y Yi PK Donahoe L Li K Miyazono P ten Dijke S Kim E Li 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 (Pubitemid 30159221)
51. DA Marchuk S Srinivasan TL Squire JS Zawistowski 2003 Vascular morphogenesis: tales of two syndromes Hum Mol Genet 12 Spec No 1 R97 112
52. P Leveen M Pekny S Gebre-Medhin B Swolin E Larsson C Betsholtz 1994 Mice deficient for PDGF B show renal, cardiovascular, and hematological abnormalities Genes Dev 8 1875 1887 (Pubitemid 24273888)
53. P Soriano 1994 Abnormal kidney development and hematological disorders in PDGF beta-receptor mutant mice Genes Dev 8 1888 1896
54. P Lindahl BR Johansson P Leveen C Betsholtz 1997 Pericyte loss and microaneurysm formation in PDGF-B-deficient mice Science 277 242 245 (Pubitemid 27446080)
55. M Hellstrom H Gerhardt M Kalen X Li U Eriksson H Wolburg C Betsholtz 2001 Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis J Cell Biol 153 543 553 (Pubitemid 34280141)
56. M Hellstrom M Kalen P Lindahl A Abramsson C Betsholtz 1999 Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse Development 126 3047 3055 (Pubitemid 29378170)
57. M Bjarnegard M Enge J Norlin S Gustafsdottir S Fredriksson A Abramsson M Takemoto E Gustafsson R Fassler C Betsholtz 2004 Endothelium-specific ablation of PDGFB leads to pericyte loss and glomerular, cardiac and placental abnormalities Development 131 1847 1857 (Pubitemid 38559851)
58. R Motiejunaite A Kazlauskas 2008 Pericytes and ocular diseases Exp Eye Res 86 171 177
59. H Gerhardt S Liebner C Redies H Wolburg 1999 N-cadherin expression in endothelial cells during early angiogenesis in the eye and brain of the chicken: relation to blood-retina and blood-brain barrier development Eur J Neurosci 11 1191 1201 (Pubitemid 29142179)
60. E Tillet D Vittet O Feraud R Moore R Kemler P Huber 2005 N-cadherin deficiency impairs pericyte recruitment, and not endothelial differentiation or sprouting, in embryonic stem cell-derived angiogenesis Exp Cell Res 310 392 400 (Pubitemid 41457342)
61. JH Paik A Skoura SS Chae AE Cowan DK Han RL Proia T Hla 2004 Sphingosine 1-phosphate receptor regulation of N-cadherin mediates vascular stabilization Genes Dev 18 2392 2403 (Pubitemid 39304686)
62. JM Rhodes M Simons 2007 The extracellular matrix and blood vessel formation: not just a scaffold J Cell Mol Med 11 176 205
63. J Lohler R Timpl R Jaenisch 1984 Embryonic lethal mutation in mouse collagen I gene causes rupture of blood vessels and is associated with erythropoietic and mesenchymal cell death Cell 38 597 607 (Pubitemid 14022052)
64. X Liu H Wu M Byrne S Krane R Jaenisch 1997 Type III collagen is crucial for collagen I fibrillogenesis and for normal cardiovascular development Proc Natl Acad Sci U S A 94 1852 1856 (Pubitemid 27113925)
65. KI Kivirikko 1993 Collagens and their abnormalities in a wide spectrum of diseases Ann Med 25 113 126 (Pubitemid 23129966)
66. R Hallmann N Horn M Selg O Wendler F Pausch LM Sorokin 2005 Expression and function of laminins in the embryonic and mature vasculature Physiol Rev 85 979 1000 (Pubitemid 40885221)
67. E Poschl U Schlotzer-Schrehardt B Brachvogel K Saito Y Ninomiya U Mayer 2004 Collagen IV is essential for basement membrane stability but dispensable for initiation of its assembly during early development Development 131 1619 1628 (Pubitemid 38559288)
68. J Thyboll J Kortesmaa R Cao R Soininen L Wang A Iivanainen L Sorokin M Risling Y Cao K Tryggvason 2002 Deletion of the laminin alpha4 chain leads to impaired microvessel maturation Mol Cell Biol 22 1194 1202 (Pubitemid 34094855)
69. JH Miner J Cunningham JR Sanes 1998 Roles for laminin in embryogenesis: exencephaly, syndactyly, and placentopathy in mice lacking the laminin alpha5 chain J Cell Biol 143 1713 1723 (Pubitemid 29006514)
70. J Golledge J Muller A Daugherty P Norman 2006 Abdominal aortic aneurysm: pathogenesis and implications for management Arterioscler Thromb Vasc Biol 26 2605 2613 (Pubitemid 44777272)
71. JD Raffetto RA Khalil 2008 Matrix metalloproteinases and their inhibitors in vascular remodeling and vascular disease Biochem Pharmacol 75 346 359 (Pubitemid 350298459)
72. GM Longo W Xiong TC Greiner Y Zhao N Fiotti BT Baxter 2002 Matrix metalloproteinases 2 and 9 work in concert to produce aortic aneurysms J Clin Invest 110 625 632 (Pubitemid 34988786)
73. JS Ikonomidis WC Gibson JE Butler DM McClister SE Sweterlitsch RP Thompson R Mukherjee FG Spinale 2004 Effects of deletion of the tissue inhibitor of matrix metalloproteinases-1 gene on the progression of murine thoracic aortic aneurysms Circulation 110 II268 273
74. S Chang BD Young S Li X Qi JA Richardson EN Olson 2006 Histone deacetylase 7 maintains vascular integrity by repressing matrix metalloproteinase 10 Cell 126 321 334 (Pubitemid 44092958)
75. R Silva G D'Amico KM Hodivala-Dilke LE Reynolds 2008 Integrins: the keys to unlocking angiogenesis Arterioscler Thromb Vasc Biol 28 1703 1713
76. BL Bader H Rayburn D Crowley RO Hynes 1998 Extensive vasculogenesis, angiogenesis, and organogenesis precede lethality in mice lacking all alpha v integrins Cell 95 507 519 (Pubitemid 28533307)
77. LE Reynolds L Wyder JC Lively D Taverna SD Robinson X Huang D Sheppard RO Hynes KM Hodivala-Dilke 2002 Enhanced pathological angiogenesis in mice lacking beta3 integrin or beta3 and beta5 integrins Nat Med 8 27 34
78. J Zhu K Motejlek D Wang K Zang A Schmidt LF Reichardt 2002 beta8 integrins are required for vascular morphogenesis in mouse embryos Development 129 2891 2903
79. JH McCarty RA Monahan-Earley LF Brown M Keller H Gerhardt K Rubin M Shani HF Dvorak H Wolburg BL Bader AM Dvorak RO Hynes 2002 Defective associations between blood vessels and brain parenchyma lead to cerebral hemorrhage in mice lacking alphav integrins Mol Cell Biol 22 7667 7677
80. JH McCarty A Lacy-Hulbert A Charest RT Bronson D Crowley D Housman J Savill J Roes RO Hynes 2005 Selective ablation of alphav integrins in the central nervous system leads to cerebral hemorrhage, seizures, axonal degeneration and premature death Development 132 165 176 (Pubitemid 40207976)
81. R Fassler M Meyer 1995 Consequences of lack of beta 1 integrin gene expression in mice Genes Dev 9 1896 1908
82. LE Stephens AE Sutherland IV Klimanskaya A Andrieux J Meneses RA Pedersen CH Damsky 1995 Deletion of beta 1 integrins in mice results in inner cell mass failure and peri-implantation lethality Genes Dev 9 1883 1895
83. L Lei D Liu Y Huang I Jovin SY Shai T Kyriakides RS Ross FJ Giordano 2008 Endothelial expression of beta1 integrin is required for embryonic vascular patterning and postnatal vascular remodeling Mol Cell Biol 28 794 802
84. S Abraham N Kogata R Fassler RH Adams 2008 Integrin beta1 subunit controls mural cell adhesion, spreading, and blood vessel wall stability Circ Res 102 562 570
85. P Labauge C Denier F Bergametti E Tournier-Lasserve 2007 Genetics of cavernous angiomas Lancet Neurol 6 237 244 (Pubitemid 46228079)
86. TL Hilder MH Malone S Bencharit J Colicelli TA Haystead GL Johnson CC Wu 2007 Proteomic identification of the cerebral cavernous malformation signaling complex J Proteome Res 6 4343 4355 (Pubitemid 350158510)
87. A Glading J Han RA Stockton MH Ginsberg 2007 KRIT-1/CCM1 is a Rap1 effector that regulates endothelial cell cell junctions J Cell Biol 179 247 254 (Pubitemid 350004889)
88. T Nitta M Hata S Gotoh Y Seo H Sasaki N Hashimoto M Furuse S Tsukita 2003 Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice J Cell Biol 161 653 660 (Pubitemid 36578587)
89. R Braren H Hu YH Kim HE Beggs LF Reichardt R Wang 2006 Endothelial FAK is essential for vascular network stability, cell survival, and lamellipodial formation J Cell Biol 172 151 162 (Pubitemid 43042637)
90. TL Shen AY Park A Alcaraz X Peng I Jang P Koni RA Flavell H Gu JL Guan 2005 Conditional knockout of focal adhesion kinase in endothelial cells reveals its role in angiogenesis and vascular development in late embryogenesis J Cell Biol 169 941 952 (Pubitemid 41002870)
91. T Shindo Y Kurihara H Nishimatsu N Moriyama M Kakoki Y Wang Y Imai A Ebihara T Kuwaki KH Ju N Minamino K Kangawa T Ishikawa M Fukuda Y Akimoto H Kawakami T Imai H Morita Y Yazaki R Nagai Y Hirata H Kurihara 2001 Vascular abnormalities and elevated blood pressure in mice lacking adrenomedullin gene Circulation 104 1964 1971 (Pubitemid 32983242)
92. KM Caron O Smithies 2001 Extreme hydrops fetalis and cardiovascular abnormalities in mice lacking a functional Adrenomedullin gene Proc Natl Acad Sci U S A 98 615 619 (Pubitemid 32105091)
93. Y Ichikawa-Shindo T Sakurai A Kamiyoshi H Kawate N Iinuma T Yoshizawa T Koyama J Fukuchi S Iimuro N Moriyama H Kawakami T Murata K Kangawa R Nagai T Shindo 2008 The GPCR modulator protein RAMP2 is essential for angiogenesis and vascular integrity J Clin Invest 118 29 39
94. AV Kwiatkowski DA Rubinson EW Dent J Edward van Veen JD Leslie J Zhang LM Mebane U Philippar EM Pinheiro AA Burds RT Bronson S Mori R Fassler FB Gertler 2007 Ena/VASP is required for neuritogenesis in the developing cortex Neuron 56 441 455 (Pubitemid 350030877)
95. C Furman AL Sieminski AV Kwiatkowski DA Rubinson E Vasile RT Bronson R Fassler FB Gertler 2007 Ena/VASP is required for endothelial barrier function in vivo J Cell Biol 179 761 775 (Pubitemid 350146260)
96. CP Regan W Li DM Boucher S Spatz MS Su K Kuida 2002 Erk5 null mice display multiple extraembryonic vascular and embryonic cardiovascular defects Proc Natl Acad Sci U S A 99 9248 9253 (Pubitemid 34764599)
97. M Hayashi SW Kim K Imanaka-Yoshida T Yoshida ED Abel B Eliceiri Y Yang RJ Ulevitch JD Lee 2004 Targeted deletion of BMK1/ERK5 in adult mice perturbs vascular integrity and leads to endothelial failure J Clin Invest 113 1138 1148 (Pubitemid 38544099)
98. F Zwerts F Lupu A De Vriese S Pollefeyt L Moons RA Altura Y Jiang PH Maxwell P Hill H Oh C Rieker D Collen SJ Conway EM Conway 2007 Lack of endothelial cell survivin causes embryonic defects in angiogenesis, cardiogenesis, and neural tube closure Blood 109 4742 4752 (Pubitemid 46827767)
99. CA Franco M Mericskay A Parlakian G Gary-Bobo J Gao-Li D Paulin E Gustafsson Z Li 2008 Serum response factor is required for sprouting angiogenesis and vascular integrity Dev Cell 15 448 461
100. A Hart F Melet P Grossfeld K Chien C Jones A Tunnacliffe R Favier A Bernstein 2000 Fli-1 is required for murine vascular and megakaryocytic development and is hemizygously deleted in patients with thrombocytopenia Immunity 13 167 177
101. C Park K Lavine Y Mishina CX Deng DM Ornitz K Choi 2006 Bone morphogenetic protein receptor 1A signaling is dispensable for hematopoietic development but essential for vessel and atrioventricular endocardial cushion formation Development 133 3473 3484 (Pubitemid 44501849)
102. J Larsson MJ Goumans LJ Sjostrand MA van Rooijen D Ward P Leveen X Xu P ten Dijke CL Mummery S Karlsson 2001 Abnormal angiogenesis but intact hematopoietic potential in TGF-beta type I receptor-deficient mice Embo J 20 1663 1673 (Pubitemid 32299403)
103. Y Lan B Liu H Yao F Li T Weng G Yang W Li X Cheng N Mao X Yang 2007 Essential role of endothelial Smad4 in vascular remodeling and integrity Mol Cell Biol 27 7683 7692 (Pubitemid 350033673)
104. X Yang LH Castilla X Xu C Li J Gotay M Weinstein PP Liu CX Deng 1999 Angiogenesis defects and mesenchymal apoptosis in mice lacking SMAD5 Development 126 1571 1580 (Pubitemid 29204322)
105. H Chang D Huylebroeck K Verschueren Q Guo MM Matzuk A Zwijsen 1999 Smad5 knockout mice die at mid-gestation due to multiple embryonic and extraembryonic defects Development 126 1631 1642 (Pubitemid 29204328)
106. T Takahashi K Takahashi PL St John PA Fleming T Tomemori T Watanabe DR Abrahamson CJ Drake T Shirasawa TO Daniel 2003 A mutant receptor tyrosine phosphatase, CD148, causes defects in vascular development Mol Cell Biol 23 1817 1831 (Pubitemid 36246061)
107. SS Foo CJ Turner S Adams A Compagni D Aubyn N Kogata P Lindblom M Shani D Zicha RH Adams 2006 Ephrin-B2 controls cell motility and adhesion during blood-vessel-wall assembly Cell 124 161 173 (Pubitemid 43069317)
108. TJ Park K Boyd T Curran 2006 Cardiovascular and craniofacial defects in Crk-null mice Mol Cell Biol 26 6272 6282 (Pubitemid 44204543)
109. AM Heegaard A Corsi CC Danielsen KL Nielsen HL Jorgensen M Riminucci MF Young P Bianco 2007 Biglycan deficiency causes spontaneous aortic dissection and rupture in mice Circulation 115 2731 2738 (Pubitemid 46842789)
110. N Nagai M Hosokawa S Itohara E Adachi T Matsushita N Hosokawa K Nagata 2000 Embryonic lethality of molecular chaperone hsp47 knockout mice is associated with defects in collagen biosynthesis J Cell Biol 150 1499 1506
111. JR Gnarra JM Ward FD Porter JR Wagner DE Devor A Grinberg MR Emmert-Buck H Westphal RD Klausner WM Linehan 1997 Defective placental vasculogenesis causes embryonic lethality in VHL-deficient mice Proc Natl Acad Sci U S A 94 9102 9107
112. N Tang F Mack VH Haase MC Simon RS Johnson 2006 pVHL function is essential for endothelial extracellular matrix deposition Mol Cell Biol 26 2519 2530