Cellular and molecular regulation of vascular permeability

Thrombosis and Haemostasis

Volumn 109, Issue 3, 2013, Pages 407-415

  Goddard, Lauren M ^a   Luisa Iruela Arispe, M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Adhesion molecules; Capillaries; Endothelial barrier; Endothelial cells; Permeability

Indexed keywords

ACTIN; ACTIVATED LEUKOCYTE CELL ADHESION MOLECULE; ANGIOPOIETIN; ANGIOPOIETIN 1; CALCIUM; CAVEOLIN 1; CLAUDIN 5; CYCLIC AMP; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GROWTH FACTOR; HISTAMINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; MEMBRANE ASSOCIATED GUANYLATE CYCLASE KINASE; NITRIC OXIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR; PROTEIN ZO1; PROTEINASE ACTIVATED RECEPTOR 1; RAC1 PROTEIN; RAP1 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; THROMBIN; TIE RECEPTOR; TRANSCRIPTION FACTOR FKHR; TUMOR NECROSIS FACTOR; UNINDEXED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN; VITRONECTIN RECEPTOR;

ARTICLE; BLOOD VESSEL PERMEABILITY; CAVEOLA; CELL ORGANELLE; ENDOTHELIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANGIOPOIETIN-1; ANIMALS; BIOLOGICAL TRANSPORT; CAPILLARIES; CAPILLARY PERMEABILITY; CELL ADHESION MOLECULES; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84874772112     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/TH12-09-0678     Document Type: Article

References (86)

1. Armulik A, Genové G, Mäe M, et al. Pericytes regulate the blood-brain barrier. Nature 2010; 468: 557-561.
2. Daneman R, Zhou L, Kebede AA, et al. Pericytes are required for blood-brain barrier integrity during embryogenesis. Nature 2010; 468: 562-566.
3. Armulik A, Genové G, Betsholtz C. Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 2011; 21: 193-215.
4. Mehta D. Signalling Mechanisms Regulating Endothelial Permeability. Physiol Rev 2006; 86: 279-367.
5. Dvorak AM, Feng D. The vesiculo-vacuolar organelle (VVO). A new endothelial cell permeability organelle. J Histochem Cytochem 2001; 49: 419-432.
6. Razani B, Engelman JA, Wang XB, et al. Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem 2001; 276: 38121-38138.
7. Schubert W, Frank PG, Razani B, et al. Caveolae-deficient endothelial cells show defects in the uptake and transport of albumin in vivo. J Biol Chem 2001; 276: 48619-48622.
8. Komarova Y, Malik AB. Regulation of endothelial permeability via paracellular and transcellular transport pathways. Annu Rev Physiol 2010; 72: 463-493.
9. Sun Y, Hu G, Zhang X et al. Phosphorylation of caveolin-1 regulates oxidant-induced pulmonary vascular permeability via paracellular and transcellular pathways. Circ Res 2009; 105: 676-685.
10. Joshi B, Bastiani M, Strgnell SS, et al. Phosphocaveolin-1 is a mechanotransducer that induces caveola biogenesis via Egr1 transcriptional regulation. J Cell Biol 2012; 199: 425-435.
11. Schubert W, Frank PG, Woodman SE, et al. Microvascular hyperpermeability in caveolin-1 (-/-) knock-out mice. Treatment with a specific nitric-oxide synthase inhibitor, L-NAME, restores normal microvascular permeability in Cav-1 null mice. J Biol Chem 2002; 277: 40091-40098.
12. Miyawaki-Shimizu K, Predescu D, Shimizu J, et al. siRNA-induced caveolin-1 knockdown in mice increases lung vascular permeability via the junctional pathway. Am J Physiol Lung Cell Mol Physiol 2006; 290: L405-413.
13. Siddiqui MR, Komarova YA, Vogel SM, et al. Caveolin-1-eNOS signalling promotes p190RhoGAP-A nitration and endothelial permeability. J Cell Biol 2011; 30: 841-850.
14. Minshall RD, Sessa WC, Stan RV, et al. Caveolin regulation of endothelial function. Am J Physiol Lung Cell Mol Physiol 2003; 285: L1179-1183.
15. Sundivakkam PC, Kwiatek AM, Sharma TT, et al. Caveolin-1 scaffold domain interacts with TRPC1 and IP3R3 to regulate Ca2+ store release-induced Ca2+ entry in endothelial cells. Am J Physiol Cell Physiol 2009; 296: C403-413.
16. Kwiatek AM, Minshall RD, Cool DR, et al. Caveolin-1 regulates store-operated Ca2+ influx by binding of its scaffolding domain to transient receptor potential channel-1 in endothelial cells. Mol Pharmacol 2006; 70: 1174-1183.
17. Marmon S, Hinchey J, Oh P, et al. Caveolin-1 Expression Determines the Route of Neutrophil Extravasation through Skin Microvasculature. Am J Pathol 2009; 174: 684-692.
18. Dejana E, Tournier-Lasserve E, Weinstein BM. The Control of Vascular Integrity by Endothelial Cell Junctions: Molecular Basis and Pathological Implications. Dev Cell 2009; 16: 209-221.
19. Dejana E, Giampietro C. Vascular endothelial-cadherin and vascular stability. Curr Opin Hematol 2012; 19: 218-223.
20. Potter MD, Barbero S, Cheresh DA. Tyrosine phosphorylation of VE-cadherin prevents binding of p120-and beta-catenin and maintains the cellular mesenchymal state. J Biol Chem 2005; 280: 31906-31912.
21. Baumeister U, Funke R, Ebnet K, et al. Association of Csk to VE-cadherin and inhibition of cell proliferation. EMBO J 2005; 24: 1686-1695.
22. Gavard J, Gutkind JS. VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin. Nat Cell Biol 2006; 8: 1223-1234.
23. Turowski P, Martinelli R, Crawford R, et al. Phosphorylation of vascular endothelial cadherin controls lymphocyte emigration. J Cell Sci 2008; 121: 29-37.
24. Orsenigo F, Giampietro C, Ferrari A, et al. Phosphorylation of VE-cadherin is modulated by haemodynamic forces and contributes to the regulation of vascular permeability in vivo. Nat Commun 2012; 3: 1208.
25. Vestweber D, Winderlich M, Cagna G, et al. Cell adhesion dynamics at endothelial junctions: VE-cadherin as a major player. Trends Cell Biol 2009; 19: 8-15.
26. Broermann A, Winderlich M, Block H, et al. Dissociation of VE-PTP from VEcadherin is required for leukocyte extravasation and for VEGF-induced vascular permeability in vivo. J Exp Med 2011; 208: 2393-2401.
27. Vandenbroucke E, Mehta D, Minshall R, et al. Regulation of Endothelial Junctional Permeability. Ann NY Acad Sci 2008; 1123: 134-145.
28. Schulte D, Kuppers V, Dartsch N, et al. Stabilising the VE-cadherin-catenin complex blocks leukocyte extravasation and vascular permeability. EMBO J 2011; 30: 4157-4170.
29. Vandenbroucke St Amant E, Tauseef M, et al. PKC_ Activation of p120-Catenin Serine 879 Phospho-Switch Disassembles VE-Cadherin Junctions and Disrupts Vascular Integrity. Circ Res 2012; 111: 739-749.
30. González-Mariscal L, Tapia R, Chamorro D. Crosstalk of tight junction components with signalling pathways. Biochim Biophys Acta 2008; 1778: 729-756.
31. Murakami T, Felinski EA, Antonetti DA. Occludin phosphorylation and ubiquitination regulate tight junction trafficking and vascular endothelial growth factor-induced permeability. J Biol Chem 2009; 284: 21036-21046.
32. Furuse M. Knockout animals and natural mutations as experimental and diagnostic tool for studying tight junction functions in vivo. Biochim Biophys Acta 2009; 1788: 813-819.
33. Orlova VV, Economopoulou M, Lupu F, et al. Junctional adhesion molecule-C regulates vascular endothelial permeability by modulating VE-cadherin-mediated cell-cell contacts. J Exp Med 2006; 203: 2703-2714.
34. Li X, Stankovic M, Lee BP, et al. JAM-C induces endothelial cell permeability through its association and regulation of {beta}3 integrins. Arterioscler Thromb Vasc Biol 2009; 29: 1200-1206.
35. Wegmann F, Petri B, Khandoga AG, et al. ESAM supports neutrophil extravasation, activation of Rho, and VEGF-induced vascular permeability. J Exp Med 2006; 203: 1671-1677.
36. Taddei A, Giampietro C, Conti A, et al. Endothelial adherens junctions control tight junctions by VE-cadherin-mediated upregulation of claudin-5. Nat Cell Biol 2008; 10: 923-934.
37. Walsh TG, Murphy RP, Fitzpatrick P, et al. Stabilisation of brain microvascular endothelial barrier function by shear stress involves VE-cadherin signalling leading to modulation of pTyr-occludin levels. J Cell Physiol 2011; 226: 3053-3063.
38. Thennes T, Mehta D. Heterotrimeric G proteins, focal adhesion kinase, and endothelial barrier function. Microvasc Res 2012 83: 31-44.
39. Chavez A, Smith M, Mehta D. New insights into the regulation of vascular permeability. Int Rev Cell Mol Biol 2011; 290: 205-248.
40. Weis SM, Cheresh DA. Pathophysiological consequences of VEGF-induced vascular permeability. Nature 2005; 437: 497-504.
41. Bates DO. Vascular endothelial growth factors and vascular permeability. Cardiovasc Res 2010; 87: 262-271.
42. Nottebaum AF, Cagna G, Winderlich M, et al. VE-PTP maintains the endothelial barrier via plakoglobin and becomes dissociated from VE-cadherin by leukocytes and by VEGF. J Exp Med 2008; 205: 2929-2945.
43. Chen XL, Nam JO, Jean C, et al. VEGF-Induced Vascular Permeability Is Mediated by FAK. Dev Cell 2012; 22: 146-157.
44. Sun Z, Li X, Massena S, et al. VEGFR2 induces c-Src signalling and vascular permeability in vivo via the adaptor protein TSAd. J Exp Med 2012; 209: 1363-1377.
45. Thibeault S, Rautureau Y, Oubaha M, et al. S-Nitrosylation of beta-Catenin by eNOS-Derived NO Promotes VEGF-Induced Endothelial Cell Permeability. Mol Cell 2010; 39: 468-476.
46. Lee SS, Jilani SM, Nikolova GV, et al. Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors. J Cell Biol 2005; 169: 681-691.
47. Chen TT, Luque A, Lee S, et al. Anchorage of VEGF to the extracellular matrix conveys differential signalling responses to endothelial cells. J Cell Biol 2010; 188: 595-609.
48. Augustin HG, Koh GY, Thurston G, et al. Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat Rev Mol Cell Biol 2009; 10: 165-177.
49. Wong AL, Haroon ZA, Werner S, et al. Tie2 expression and phosphorylation in angiogenic and quiescent adult tissues. Circ Res 1997; 81: 567-574
50. Thurston G, Rudge JS, Ioffe E, et al. Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat Med 2000; 6: 460-463.
51. Mammoto T, Parikh SM, Mammoto A, et al. Angiopoietin-1 requires p190 Rho-GAP to protect against vascular leakage in vivo. J Biol Chem 2007; 282: 23910-23918.
52. Gavard J, Patel V, Gutkind JS. Angiopoietin-1 prevents VEGF-induced endothelial permeability by sequestering Src through mDia. Dev Cell 2008; 14: 25-36.
53. Jho D, Mehta D, Ahmmed G, et al. Angiopoietin-1 Opposes VEGF-Induced Increase in Endothelial Permeability by Inhibiting TRPC1-Dependent Ca2 Influx. Circ Res. 2005; 96: 1282-90.
54. Oubaha M, Gratton JP. Phosphorylation of endothelial nitric oxide synthase by atypical PKC zeta contributes to angiopoietin-1-dependent inhibition of VEGFinduced endothelial permeability in vitro. Blood 2009; 114: 3343-3351.
55. Saharinen P, Eklund L, Miettinen J, et al. Angiopoietins assemble distinct Tie2 signalling complexes in endothelial cell-cell and cell-matrix contacts. Nat Cell Biol 2008; 10: 527-537.
56. Fukuhara S, Sako K, Minami T, et al. Differential function of Tie2 at cell-cell contacts and cell-substratum contacts regulated by angiopoietin-1. Nat Cell Biol 2008; 10: 513-526.
57. Scharpfenecker M, Fiedler U, Reiss Y, et al. The Tie-2 ligand angiopoietin-2 destabilizes quiescent endothelium through an internal autocrine loop mechanism. J. Cell Sci 2005; 118: 771-780.
58. Thomas M, Felcht M, Kruse K, et al. Angiopoietin-2 stimulation of endothelial cells induces alphavbeta3 integrin internalisation and degradation. J Biol Chem 2010; 285: 23842-23849.
59. Yuan HT, Khankin EV, Karumanchi SA, et al. Angiopoietin 2 is a partial agonist/ antagonist of Tie2 signalling in the endothelium. Mol Cell Biol 2009; 29: 2011-2022.
60. Harfouche R, Hussain SN. Signalling and regulation of endothelial cell survival by angiopoietin-2. Am J Physiol Heart Circ Physiol 2006; 291: H1635-1645.
61. Daly C, Pasnikowski E, Burova E, et al. Angiopoietin-2 functions as an autocrine protective factor in stressed endothelial cells. Proc Natl Acad Sci USA 2006; 103: 15491-15496.
62. Knezevic N, Tauseef M, Thennes T, et al. The G protein betagamma subunit mediates reannealing of adherens junctions to reverse endothelial permeability increase by thrombin. J Exp Med 2009; 206: 2761-2777.
63. Cullere X, Shaw SK, Andersson L, et al. Regulation of vascular endothelial barrier function by Epac, a cAMP-activated exchange factor for Rap GTPase. Blood 2005; 105: 1950-1955.
64. Fukuhara S, Sakurai A, Sano H, et al. Cyclic AMP potentiates vascular endothelial cadherin-mediated cell-cell contact to enhance endothelial barrier function through an Epac-Rap1 signalling pathway. Mol Cell Biol 2005; 25: 136-146.
65. Kooistra MR, Dube N, Bos JL. Rap1: a key regulator in cell-cell junction formation. J Cell Sci 2007; 120: 17-22.
66. Glading A, Han J, Stockton RA, et al. KRIT-1/CCM1 is a Rap1 effector that regulates endothelial cell cell junctions. J Cell Biol 2007; 179: 247-254.
67. Murakami M, Nguyen LT, Zhuang ZW, et al. The FGF system has a key role in regulating vascular integrity. J Clin Invest 2008; 118: 3355-3366.
68. Hatanaka K, Lanahan A, Murakami M, et al. Fibroblast Growth Factor Signalling Potentiates VE-Cadherin Stability at Adherens Junctions by Regulating SHP2. PLoS One 2012; 7: e37600.
69. Sun X, Shikata Y, Wang L, et al. Enhanced interaction between focal adhesion and adherens junction proteins: involvement in sphingosine 1-phosphate-induced endothelial barrier enhancement. Microvasc Res 2009; 77: 304-313.
70. Jung B, Obinata H, Galvani S et al. Flow-regulated endothelial S1P receptor-1 signalling sustains vascular development. Dev Cell 2012; 23: 600-610.
71. Gaengel K, Niaudet C, Hagikura K et al. The sphingosine-1-phosphate receptor S1PR1 restricts sprouting angiogenesis by regulating the interplay between VEcadherin and VEGFR2. Dev Cell 2012; 23: 587-599.
72. Shikata Y, Birukov KG, Garcia JG. S1P induces FA remodelling in human pulmonary endothelial cells: role of Rac, GIT1, FAK, and paxillin. J Appl Physiol 2003; 94: 1193-1203.
73. Guo M, Wu MH, Granger HJ, et al. Focal adhesion kinase in neutrophil-induced microvascular hyperpermeability. Microcirculation 2005; 12: 223-232.
74. Lee YH, Kayyali US, Sousa AM, et al. Transforming growth factor-beta1 effects on endothelial monolayer permeability involve focal adhesion kinase/Src. Am J Respir Cell Mol Biol. 2007; 37: 485-493.
75. Belvitch P, Dudek SM. Role of FAK in S1P-regulated endothelial permeability. Microvasc Res 2012; 83: 22-30.
76. Shikata Y, Birukov KG, Birukova AA, et al. Involvement of site-specific FAK phosphorylation in sphingosine-1 phosphate-and thrombin-induced focal adhesion remodelling: role of Src and GIT. FASEB J 2003; 17: 2240-2249.
77. Daly C, Wong V, Burova E, et al. Angiopoietin-1 modulates endothelial cell function and gene expression via the transcription factor FKHR (FOXO1). Genes Dev 2004; 18: 1060-1071.
78. Dixit M, Bess E, Fisslthaler B, et al. Shear stress-induced activation of the AMPactivated protein kinase regulates FoxO1a and angiopoietin-2 in endothelial cells. Cardiovasc Res 2008; 77: 160-168.
79. Cowan CE, Kohler EE, Dugan TA, et al. Kruppel-Like Factor-4 Transcriptionally Regulates VE-Cadherin Expression and Endothelial Barrier Function. Circ Res. 2010; 107: 959-966.
80. Lin Z, Natesan V, Shi H, et al. Kruppel-like factor 2 regulates endothelial barrier function. Arterioscler Thromb Vasc Biol 2010; 30: 1952-1959.
81. Haidari M, Zhang W, Chen Z, et al. Myosin light chain phosphorylation facilitates monocyte transendothelial migration by dissociating endothelial adherens junctions. Cardiovasc Res 2011; 92: 456-465.
82. David S, Ghosh CC, Mukherjee A, et al. Angiopoietin-1 Requires IQ Domain GTPase-Activating Protein 1 to Activate Rac1 and Promote Endothelial Barrier Defense. Arterioscler Thromb Vasc Biol 2011; 31: 2643-2652.
83. Peng J, He F, Zhang C, et al. Protein kinase Ca signals P115RhoGEF phosphorylation and RhoA activation in TNF-a-induced mouse brain microvascular endothelial cell barrier dysfunction. J Neuroinflammation 2011; 8: 28.
84. Chava KR, Tauseef M, Sharma T, et al. Cyclic AMP response element binding (CREB) protein prevents endothelial permeability increase through transcriptional controlling p190RhoGAP expression. Blood 2012; 119: 308-319.
85. Zhao D, Qin L, Bourbon PM, et al. Orphan nuclear transcription factor TR3/Nur77 regulates microvessel permeability by targeting endothelial nitric oxide synthase and destabilising endothelial junctions. Proc Natl Acad Sci USA 2011; 108: 12066-12071.
86. Burek M, Arias-Loza PA, Roewer N, et al. Claudin-5 as a novel estrogen target in vascular endothelium. Arterioscler Thromb Vasc Biol 2010; 30: 298-304.