Crossing the wall: The opening of endothelial cell junctions during infectious diseases

International Journal of Biochemistry and Cell Biology

Volumn 45, Issue 7, 2013, Pages 1165-1173

  Razakandrainibe, Romy ^a   Combes, Valery ^b   Grau, Georges E ^b   Jambou, Ronan ^a  

^a INSTITUT PASTEUR DE MADAGASCAR   (Madagascar)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Dengue; Endothelial cell; Intercellular junction; Malaria; Transcytose

Indexed keywords

HISTAMINE;

APOPTOSIS; BACTERIUM; CELL ADHESION; CELL JUNCTION; CELL MEMBRANE PERMEABILITY; CELL MIGRATION; CENTRAL NERVOUS SYSTEM; EDEMA; ENDOTHELIUM; ENDOTHELIUM CELL; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; INFECTION; MOLECULE; NONHUMAN; PATHOLOGY; PLASMODIUM; REVIEW; TOXOPLASMA GONDII; COMMUNICABLE DISEASE; IMMUNOLOGY; INFLAMMATION; METABOLISM; MICROBIOLOGY; PARASITOLOGY; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; VASCULAR ENDOTHELIUM; VIROLOGY;

APOPTOSIS; CELL ADHESION; COMMUNICABLE DISEASES; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; INFLAMMATION; INTERCELLULAR JUNCTIONS; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION;

EID: 84877052461     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2013.03.010     Document Type: Review

References (102)

1. K. Abe, and M. Takeichi EPLIN mediates linkage of the cadherin catenin complex to F-actin and stabilizes the circumferential actin belt Proceedings of the National Academy of Sciences of the United States of America 105 1 2008 13 19
2. P. Alcaide, S. Auerbach, and F.W. Luscinskas Neutrophil recruitment under shear flow: it's all about endothelial cell rings and gaps Microcirculation 16 1 2009 43 57
3. H. Beekhuizen, J.S. Van De Gevel, B. Olsson, I.J. Van Benten, and R. Van Furth Infection of human vascular endothelial cells with Staphylococcus aureus induces hyperadhesiveness for human monocytes and granulocytes Journal of Immunology 158 2 1997 774 782 (Pubitemid 127492654)
4. G. Benais-Pont, A. Punn, C. Flores-Maldonado, J. Eckert, G. Raposo, and T.P. Fleming Identification of a tight junction-associated guanine nucleotide exchange factor that activates Rho and regulates paracellular permeability Journal of Cell Biology 160 5 2003 729 740 (Pubitemid 36298268)
5. J.P. Blackburn, N.S. Peters, H.I. Yeh, S. Rothery, C.R. Green, and N.J. Severs Upregulation of connexin43 gap junctions during early stages of human coronary atherosclerosis Arteriosclerosis, Thrombosis, and Vascular Biology 15 8 1995 1219 1228
6. C.S. Bonder, S.R. Clark, M.U. Norman, P. Johnson, and P. Kubes Use of CD44 by CD4+ Th1 and Th2 lymphocytes to roll and adhere Blood 107 12 2006 4798 4806 (Pubitemid 43882631)
7. H. Brown, T.T. Hien, N. Day, N.T. Mai, L.V. Chuong, and T.T. Chau Evidence of blood-brain barrier dysfunction in human cerebral malaria Neuropathology and Applied Neurobiology 25 4 1999 331 340 (Pubitemid 29392713)
8. T.M. Calderon, S.D. Gertz, I.J. Sarembock, J.A. Berliner, J.T. Fallon, and M.B. Taubman Induction of IG9 monocyte adhesion molecule expression in smooth muscle and endothelial cells after balloon arterial injury in cholesterol-fed rabbits Arteriosclerosis, Thrombosis, and Vascular Biology 20 5 2000 1293 1300 (Pubitemid 30262930)
9. S.B. Campos, S.L. Ashworth, S. Wean, M. Hosford, R.M. Sandoval, and M.A. Hallett Cytokine-induced F-actin reorganization in endothelial cells involves RhoA activation American Journal of Physiology. Renal Physiology 296 3 2009 F487 F495 Epub 2009 Jan 2014.
10. V. Combes, T.E. Taylor, I. Juhan-Vague, J.L. Mège, J. Mwenechanya, and M. Tembo Circulating endothelial microparticles in Malawian children with severe falciparum malaria complicated with coma Journal of the American Medical Association 291 21 2004 2542 2544 (Pubitemid 38702769)
11. D.O.J. Zamora, T. Rosenbaum, and J.R. Smith Invasion of human retinal vascular endothelial cells by Toxoplasma gondii tachyzoites British Journal of Ophthalmology 92 2008 852 855 (Pubitemid 351839583)
12. W. Däubener, B. Spors, C. Hucke, R. Adam, M. Stins, and K. Ks Restriction of Toxoplasma gondii growth in human brain microvascular endothelial cells by activation of indoleamine 2,3-dioxygenase Infection and Immunity 69 2001 6527 6531 (Pubitemid 32885221)
13. M.J. Davies, J.L. Gordon, A.J. Gearing, R. Pigott, N. Woolf, and D. Katz The expression of the adhesion molecules ICAM-1, VCAM-1 PECAM, and E-selectin in human atherosclerosis Journal of Pathology 171 3 1993 223 229 (Pubitemid 23345967)
14. E. Dejana, F. Breviario, and L. Caveda Leukocyte-endothelial cell adhesive receptors Clinical and Experimental Rheumatology 12 Suppl. 10 1994 S25 S28
15. Y. Delneste, P. Lassalle, P. Jeannin, M. Joseph, A.B. Tonnel, and P. Gosset Histamine induces IL-6 production by human endothelial cells Clinical and Experimental Immunology 98 2 1994 344 349 (Pubitemid 24336836)
16. G.L. Dixon, R.S. Heyderman, K. Kotovicz, D.L. Jack, S.R. Andersen, and U. Vogel Endothelial adhesion molecule expression and its inhibition by recombinant bactericidal/permeability-increasing protein are influenced by the capsulation and lipooligosaccharide structure of Neisseria meningitidis Infection and Immunity 67 11 1999 5626 5633 (Pubitemid 29508079)
17. N. Doulet, E. Donnadieu, M.P. Laran-Chich, F. Niedergang, X. Nassif, and P.O. Couraud Neisseria meningitidis infection of human endothelial cells interferes with leukocyte transmigration by preventing the formation of endothelial docking structures Journal of Cell Biology 173 4 2006 627 637 (Pubitemid 43765207)
18. F. Drees, S. Pokutta, S. Yamada, W.J. Nelson, and W.I. Weis Alpha-catenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actin-filament assembly Cell 123 5 2005 903 915 (Pubitemid 41721035)
19. H.M. Elsheikha, and N.A. Khan Protozoa traversal of the blood-brain barrier to invade the central nervous system FEMS Microbiology Review 34 2010 532 553
20. B. Engelhardt Regulation of immune cell entry into the central nervous system Results and Problems in Cell Differentiation 43 2006 259 280 (Pubitemid 44445588)
21. C.W. Esslinger, S. Picot, and P. Ambroise-Thomas Intra-erythrocytic Plasmodium falciparum induces up-regulation of inter-cellular adhesion molecule-1 on human endothelial cells in vitro Scandinavian Journal of Immunology 39 3 1994 229 232 (Pubitemid 24203075)
22. X.F. Figueroa, and B.R. Duling Gap junctions in the control of vascular function Antioxidants and Redox Signalling 11 2 2009 251 266
23. P.S. Frenette, C.V. Denis, L. Weiss, K. Jurk, S. Subbarao, and B. Kehrel P-Selectin glycoprotein ligand 1 (PSGL-1) is expressed on platelets and can mediate platelet-endothelial interactions in vivo Journal of Experimental Medicine 191 8 2000 1413 1422 (Pubitemid 30227127)
24. J. Gavard, and J.S. Gutkind VEGF controls endothelial-cell permeability by promoting the beta-arrestin-dependent endocytosis of VE-cadherin Nature Cell Biology 8 11 2006 1223 1234 (Pubitemid 44660587)
25. J. Gavard, and J.S. Gutkind VE-cadherin and claudin-5: it takes two to tango Nature Cell Biology 10 8 2008 883 885
26. P. Gong, D.J. Angelini, S. Yang, G. Xia, A.S. Cross, and D. Mann TLR4 signaling is coupled to SRC family kinase activation, tyrosine phosphorylation of zonula adherens proteins, and opening of the paracellular pathway in human lung microvascular endothelia Journal of Biological Chemistry 283 19 2008 13437 13449
27. G.E. Grau, E. Terrie, D.O. Taylor, M.E. Molyneux, J.J. Wirima, and P. Vassalli Tumor necrosis factor and disease severity in children with falciparum malaria New England Journal of Medicine 320 1989 1586 1591 (Pubitemid 19154572)
28. G.E. Grau, C.D. Mackenzie, R.A. Carr, M. Redard, G. Pizzolato, and C. Allasia Platelet accumulation in brain microvessels in fatal pediatric cerebral malaria Journal of Infectious Diseases 187 3 2003 461 466 (Pubitemid 36184587)
29. S.B. Halstead Dengue Lancet 370 9599 2007 1644 1652 (Pubitemid 350052290)
30. R.J. Hamill, J.M. Vann, and R.A. Proctor Phagocytosis of Staphylococcus aureus by cultured bovine aortic endothelial cells: model for postadherence events in endovascular infections Infection and Immunity 54 3 1986 833 836 (Pubitemid 17186458)
31. B.T. Hawkins, and T.P. Davis The blood-brain barrier/neurovascular unit in health and disease Pharmacological Reviews 57 2 2005 173 185 (Pubitemid 41043883)
32. P. Heeringa, D. Huugen, and J.W. Tervaert Anti-neutrophil cytoplasmic autoantibodies and leukocyte-endothelial interactions: a sticky connection? Trends in Immunology 26 11 2005 561 564 (Pubitemid 41726442)
33. V. Henn, J.R. Slupsky, M. Grafe, I. Anagnostopoulos, R. Forster, and G. Muller-Berghaus CD40 ligand on activated platelets triggers an inflammatory reaction of endothelial cells Nature 391 6667 1998 591 594 (Pubitemid 28157601)
34. W.F. Hickey, B.L. Hsu, and H. Kimura T-lymphocyte entry into the central nervous system Journal of Neuroscience Research 28 2 1991 254 260
35. T. Hirase, S. Kawashima, E.Y. Wong, T. Ueyama, Y. Rikitake, and S. Tsukita Regulation of tight junction permeability and occludin phosphorylation by Rhoa-p160ROCK-dependent and -independent mechanisms Journal of Biological Chemistry 276 13 2001 10423 10431
36. I. Hoffmann, E. Eugene, X. Nassif, P.O. Couraud, and S. Bourdoulous Activation of ErbB2 receptor tyrosine kinase supports invasion of endothelial cells by Neisseria meningitidis Journal of Cell Biology 155 1 2001 133 143 (Pubitemid 34286214)
37. M.J. Hollestelle, C. Donkor, E.A. Mantey, S.J. Chakravorty, A. Craig, and A.O. Akoto von Willebrand factor propeptide in malaria: evidence of acute endothelial cell activation British Journal of Haematology 133 5 2006 562 569
38. R. Horuk, A. Martin, J. Hesselgesser, T. Hadley, Z.H. Lu, and Z.X. Wang The Duffy antigen receptor for chemokines: structural analysis and expression in the brain Journal of Leukocyte Biology 59 1 1996 29 38 (Pubitemid 26057472)
39. M.B. Huang, M. Khan, M. Garcia-Barrio, M. Powell, and V.C. Bond Apoptotic effects in primary human umbilical vein endothelial cell cultures caused by exposure to virion-associated and cell membrane-associated HIV-1 gp120 Journal of Acquired Immune Deficiency Syndromes 27 3 2001 213 221 (Pubitemid 32661961)
40. R.R. Johnson-Tidey, J.L. Mcgregor, P.R. Taylor, and R.N. Poston Increase in the adhesion molecule P-selectin in endothelium overlying atherosclerotic plaques Coexpression with intercellular adhesion molecule-1 American Journal of Pathology 144 5 1994 952 961 (Pubitemid 24160636)
41. H. Kallstrom, M.K. Liszewski, J.P. Atkinson, and A.B. Jonsson Membrane cofactor protein (MCP or CD46) is a cellular pilus receptor for pathogenic Neisseria Molecular Microbiology 25 4 1997 639 647 (Pubitemid 27394562)
42. G.D. Kanmogne, R.C. Kennedy, and P. Grammas HIV-1 gp120 proteins and gp160 peptides are toxic to brain endothelial cells and neurons: possible pathway for HIV entry into the brain and HIV-associated dementia Journal of Neuropathology and Experimental Neurology 61 11 2002 992 1000 (Pubitemid 35278721)
43. G.D. Kanmogne, C. Primeaux, and P. Grammas HIV-1 gp120 proteins alter tight junction protein expression and brain endothelial cell permeability: implications for the pathogenesis of HIV-associated dementia Journal of Neuropathology and Experimental Neurology 64 6 2005 498 505 (Pubitemid 40781152)
44. H. Kido, J. Chida, M. Yao, and S. Wang Mechanisms of multi-organ failure in severe influenza Nihon Rinsho 68 8 2010 1565 1573
45. H. Kido, Y. Okumura, E. Takahashi, H.Y. Pan, S. Wang, and D. Yao Role of host cellular proteases in the pathogenesis of influenza and influenza-induced multiple organ failure Biochimica et Biophysica Acta 1824 1 2012 186 194
46. I.I. Knezevic, S.A. Predescu, R.F. Neamu, M.S. Gorovoy, N.M. Knezevic, and C. Easington Tiam1 and Rac1 are required for platelet-activating factor-induced endothelial junctional disassembly and increase in vascular permeability Journal of Biological Chemistry 284 8 2009 5381 5394
47. U. Kniesel, and H. Wolburg Tight junctions of the blood-brain barrier Cellular and Molecular Neurobiology 20 1 2000 57 76 (Pubitemid 30090916)
48. A. Kobielak, and E. Fuchs Alpha-catenin: at the junction of intercellular adhesion and actin dynamics Nature Reviews Molecular Cell Biology 5 8 2004 614 625 (Pubitemid 39025062)
49. S.M. Lachenmaier, M.A. Deli, M. Meissner, and O. Liesenfeld Intracellular transport of Toxoplasma gondii through the blood-brain barrier Journal of Neuroimmunology 232 2011 119 130
50. S. Lantero, G. Alessandri, D. Spallarossa, L. Scarso, and G.A. Rossi Stimulation of eosinophil IgE low-affinity receptor leads to increased adhesion molecule expression and cell migration European Respiratory Journal 16 5 2000 940 946 (Pubitemid 32049383)
51. E. Larsen, A. Celi, G.E. Gilbert, B.C. Furie, J.K. Erban, and R. Bonfanti PADGEM protein: a receptor that mediates the interaction of activated platelets with neutrophils and monocytes Cell 59 2 1989 305 312 (Pubitemid 19264376)
52. E. Larsen, T. Palabrica, S. Sajer, G.E. Gilbert, D.D. Wagner, and B.C. Furie PADGEM-dependent adhesion of platelets to monocytes and neutrophils is mediated by a lineage-specific carbohydrate, LNF III (CD15) Cell 63 3 1990 467 474
53. D. Leckband Beyond structure: mechanism and dynamics of intercellular adhesion Biochemical Society Transactions 36 Pt. 2 2008 213 220 (Pubitemid 351570592)
54. D. Leckband, and A. Prakasam Mechanism and dynamics of cadherin adhesion Annual Review of Biomedical Engineering 8 2006 259 287 (Pubitemid 44314818)
55. A.C. Luissint, P.G. Lutz, D.A. Calderwood, P.O. Couraud, and S. Bourdoulous JAM-L-mediated leukocyte adhesion to endothelial cells is regulated in cis by alpha4beta1 integrin activation Journal of Cell Biology 183 6 2008 1159 1173
56. S.M. Macdonald, J. Bhisutthibhan, T.A. Shapiro, S.J. Rogerson, T.E. Taylor, and M. Tembo Immune mimicry in malaria: Plasmodium falciparum secretes a functional histamine-releasing factor homolog in vitro and in vivo Proceedings of the National Academy of Sciences of the United States of America 98 19 2001 10829 10832 (Pubitemid 32878705)
57. S.M. Macdonald, T. Rafnar, J. Langdon, and L.M. Lichtenstein Molecular identification of an IgE-dependent histamine-releasing factor Science 269 5224 1995 688 690
58. Z. Mamdouh, A. Mikhailov, and W.A. Muller Transcellular migration of leukocytes is mediated by the endothelial lateral border recycling compartment Journal of Experimental Medicine 206 12 2009 2795 2808
59. S. Marmon, J. Hinchey, P. Oh, M. Cammer, C.J. De Almeida, and L. Gunther Caveolin-1 expression determines the route of neutrophil extravasation through skin microvasculature American Journal of Pathology 174 2 2009 684 692
60. I. Martin-Padura, S. Lostaglio, M. Schneemann, L. Williams, M. Romano, and P. Fruscella Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration Journal of Cell Biology 142 1 1998 117 127 (Pubitemid 28341144)
61. A. Matussek, J. Strindhall, L. Stark, M. Rohde, R. Geffers, and J. Buer Infection of human endothelial cells with Staphylococcus aureus induces transcription of genes encoding an innate immunity response Scandinavian Journal of Immunology 61 6 2005 536 544 (Pubitemid 40897109)
62. A. Mazzoni, H.A. Young, J.H. Spitzer, A. Visintin, and D.M. Segal Histamine regulates cytokine production in maturing dendritic cells, resulting in altered T cell polarization Journal of Clinical Investigation 108 12 2001 1865 1873 (Pubitemid 34015132)
63. W. Mcguire, A.V. Hill, B.M. Greenwood, and D. Kwiatkowski Circulating ICAM-1 levels in falciparum malaria are high but unrelated to disease severity Transactions of the Royal Society of Tropical Medicine and Hygiene 90 3 1996 274 276 (Pubitemid 26188872)
64. D. Mehta, and A.B. Malik Signaling mechanisms regulating endothelial permeability Physiological Reviews 86 1 2006 279 367
65. I. Miki, A. Kusano, S. Ohta, N. Hanai, M. Otoshi, and S. Masaki Histamine enhanced the TNF-alpha-induced expression of E-selectin and ICAM-1 on vascular endothelial cells Cellular Immunology 171 2 1996 285 288 (Pubitemid 26268486)
66. P. Mina-Osorio, B. Winnicka, C. O'conor, C.L. Grant, L.K. Vogel, and D. Rodriguez-Pinto CD13 is a novel mediator of monocytic/endothelial cell adhesion Journal of Leukocyte Biology 84 2 2008 448 459
67. D. Nantakomol, A.M. Dondorp, S. Krudsood, R. Udomsangpetch, K. Pattanapanyasat, and V. Combes Circulating red cell-derived microparticles in human malaria Journal of Infectious Diseases 203 5 2011 700 706
68. X. Nassif, S. Bourdoulous, E. Eugene, and P.O. Couraud How do extracellular pathogens cross the blood-brain barrier? Trends in Microbiology 10 5 2002 227 232 (Pubitemid 34327815)
69. S. Ohtsuki, H. Yamaguchi, Y. Katsukura, T. Asashima, and T. Terasaki Tetsuya, and mRNA expression levels of tight junction protein genes in mouse brain capillary endothelial cells highly purified by magnetic cell sorting Journal of Neurochemistry 104 1 2008 147 154 (Pubitemid 350265064)
70. A.W. Orr, R. Stockton, M.B. Simmers, J.M. Sanders, I.J. Sarembock, and B.R. Blackman Matrix-specific p21-activated kinase activation regulates vascular permeability in atherogenesis Journal of Cell Biology 176 5 2007 719 727 (Pubitemid 46333985)
71. J.B. Pankoui Mfonkeu, I. Gouado, H. Fotso Kuaté, O. Zambou, P.H. Amvam Zollo, and G.E. Grau Elevated cell-specific microparticles are a biological marker for cerebral dysfunctions in human severe malaria PLoS ONE 5 10 2010 e13415
72. P. André, D. Hartwell, I. Hrachovinová, S. Saffaripour, and D.D. Wagner Pro-coagulant state resulting from high levels of soluble P-selectin in blood Proceedings of the National Academy of Sciences of the United States of America 97 25 2000 13835 13840
73. S. Pelleau, S. Diop, M. Dia Badiane, J. Vitte, P. Beguin, and F. Nato Enhanced basophil reactivities during severe malaria and their relationship with the Plasmodium falciparum histamine-releasing factor translationally controlled tumor protein Infection and Immunity 80 8 2012 2963 2970 Epub 2012 July
74. H. Perlmann, H. Helmby, M. Hagstedt, J. Carlson, P.H. Larsson, and M. Troye-Blomberg IgE elevation and IgE anti-malarial antibodies in Plasmodium falciparum malaria: association of high IgE levels with cerebral malaria Clinical and Experimental Immunology 97 2 1994 284 292 (Pubitemid 24263072)
75. P. Perlmann, H. Perlmann, B.W. Flyg, M. Hagstedt, G. Elghazali, and S. Worku a pathogenic factor in Plasmodium falciparum malaria Infection and Immunity 65 1 1997 116 121 (Pubitemid 27008911)
76. Y. Persidsky, and H.E. Gendelman Mononuclear phagocyte immunity and the neuropathogenesis of HIV-1 infection Journal of Leukocyte Biology 74 5 2003 691 701 (Pubitemid 38040345)
77. P. Pino, J. Nitcheu, and D. Mazier Cerebral malaria, a key role for endothelial cells? Journal de la Societe de Biologie 198 3 2004 187 192
78. E. Pongponratn, M. Riganti, B. Punpoowong, and M. Aikawa Microvascular sequestration of parasitized erythrocytes in human falciparum malaria: a pathological study American Journal of Tropical Medicine and Hygiene 44 2 1991 168 175
79. R. Razakandrainibe, S. Pelleau, G.E. Grau, and R. Jambou Antigen presentation by endothelial cells: what role in the pathophysiology of malaria? Trends in Parasitology 28 4 2012 151 160
80. T. Romani De Wit, H.P. De Leeuw, M.G. Rondaij, R.T. De Laaf, E. Sellink, and H.J. Brinkman Von Willebrand factor targets IL-8 to Weibel-Palade bodies in an endothelial cell line Experimental Cell Research 286 1 2003 67 74 (Pubitemid 36506859)
81. A. Rot Contribution of Duffy antigen to chemokine function Cytokine and Growth Factor Reviews 16 6 2005 687 694 (Pubitemid 41505524)
82. N. Rudini, A. Felici, C. Giampietro, M. Lampugnani, M. Corada, and K. Swirsding VE-cadherin is a critical endothelial regulator of TGF-beta signalling EMBO Journal 27 7 2008 993 1004 (Pubitemid 351508155)
83. B. Schulz, J. Pruessmeyer, T. Maretzky, A. Ludwig, C.P. Blobel, and P. Saftig ADAM10 regulates endothelial permeability and T-Cell transmigration by proteolysis of vascular endothelial cadherin Circulation Research 102 10 2008 1192 1201
84. A. Shigeta, M. Matsumoto, T.F. Tedder, J.B. Lowe, M. Miyasaka, and T. Hirata An L-selectin ligand distinct from P-selectin glycoprotein ligand-1 is expressed on endothelial cells and promotes neutrophil rolling in inflammation Blood 112 13 2008 4915 4923
85. M.H. Siegelman, H.C. Degrendele, and P. Estess Activation and interaction of CD44 and hyaluronan in immunological systems Journal of Leukocyte Biology 66 2 1999 315 321 (Pubitemid 29379176)
86. A. Smorodchenko, J. Wuerfel, E.E. Pohl, J. Vogt, E. Tysiak, and R. Glumm CNS-irrelevant T-cells enter the brain, cause blood-brain barrier disruption but no glial pathology European Journal of Neuroscience 26 6 2007 1387 1398 (Pubitemid 47416537)
87. S.M. Stamatovic, R.F. Keep, S.L. Kunkel, and A.V. Andjelkovic Potential role of MCP-1 in endothelial cell tight junction 'opening': signaling via Rho and Rho kinase Journal of Cell Science 116 Pt 22 2003 4615 4628 (Pubitemid 37461616)
88. T. Stevens, J.G. Garcia, D.M. Shasby, J. Bhattacharya, and A.B. Malik Mechanisms regulating endothelial cell barrier function American Journal of Physiology. Lung Cellular and Molecular Physiology 279 3 2000 L419 L422
89. R.A. Stockton, E. Schaefer, and M.A. Schwartz p21-activated kinase regulates endothelial permeability through modulation of contractility Journal of Biological Chemistry 279 45 2004 46621 46630 (Pubitemid 39518307)
90. G.L. Suidan, J.R. Mcdole, Y. Chen, I. Pirko, and A.J. Johnson Induction of blood-brain barrier tight junction protein alterations by CD8 T cells PLoS ONE 3 8 2008 e3037
91. A. Taddei, C. Giampietro, A. Conti, F. Orsenigo, F. Breviario, and V. Pirazzoli Endothelial adherens junctions control tight junctions by VE-cadherin-mediated upregulation of claudin-5 Nature Cell Biology 10 8 2008 923 934
92. M.K. Taha Neisseria meningitidis induces the expression of the TNF-alpha gene in endothelial cells Cytokine 12 1 2000 21 25
93. M. Toborek, Y.W. Lee, G. Flora, H. Pu, I.E. Andras, and E. Wylegala Mechanisms of the blood-brain barrier disruption in HIV-1 infection Cellular and Molecular Neurobiology 25 1 2005 181 199 (Pubitemid 40558590)
94. S. Tsukita, M. Furuse, and M. Itoh Multifunctional strands in tight junctions Nature Reviews Molecular Cell Biology 2 4 2001 285 293 (Pubitemid 33676971)
95. G.P. Van Nieuw Amerongen, and V.W. Van Hinsbergh Targets for pharmacological intervention of endothelial hyperpermeability and barrier function Vascular Pharmacology 39 4-5 2002 257 272 (Pubitemid 37490751)
96. D. Vestweber VE-cadherin: the major endothelial adhesion molecule controlling cellular junctions and blood vessel formation Arteriosclerosis, Thrombosis, and Vascular Biology 28 2 2008 223 232 (Pubitemid 351161193)
97. S.C. Wassmer, J.B. De Souza, C. Frère, F.J. Candal, I. Juhan-Vague, and G. Ge TGF-beta1 released from activated platelets can induce TNF-stimulated human brain endothelium apoptosis: a new mechanism for microvascular lesion during cerebral malaria Journal of Immunology 176 2 2006 1180 1184 (Pubitemid 43099721)
98. B. Wojciak-Stothard, A. Entwistle, R. Garg, and R. Aj Regulation of TNF-alpha-induced reorganization of the actin cytoskeleton and cell-cell junctions by Rho, Rac, and Cdc42 in human endothelial cells Journal of Cellular Physiology 176 1998 150 165 (Pubitemid 28277205)
99. K. Xiao, J. Garner, K.M. Buckley, P.A. Vincent, C.M. Chiasson, and E. Dejana p120-Catenin regulates clathrin-dependent endocytosis of VE-cadherin Molecular Biology of the Cell 16 11 2005 5141 5151 (Pubitemid 41566827)
100. L. Yang, R.M. Froio, T.E. Sciuto, A.M. Dvorak, R. Alon, and F.W. Luscinskas ICAM-1 regulates neutrophil adhesion and transcellular migration of TNF-alpha-activated vascular endothelium under flow Blood 106 2 2005 584 592 (Pubitemid 40981255)
101. M.J. Yellin, J. Brett, D. Baum, A. Matsushima, M. Szabolcs, and D. Stern Functional interactions of T cells with endothelial cells: the role of CD40L-CD40-mediated signals Journal of Experimental Medicine 182 6 1995 1857 1864
102. A.L. Zozulya, and H. Wiendl The role of CD8 suppressors versus destructors in autoimmune central nervous system inflammation Human Immunology 69 11 2008 797 804