Phosphatases and kinases as regulators of the endothelial barrier function

Cell and Tissue Research

Volumn 355, Issue 3, 2014, Pages 577-586

  Küppers, Verena ^a   Vockel, Matthias ^a   Nottebaum, Astrid F ^a   Vestweber, Dietmar ^a  

^a MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

Author keywords

Endothelium; Kinases; Phosphatases; Phosphorylation; VE PTP

Indexed keywords

PHOSPHATASE; PHOSPHOTRANSFERASE;

ANIMAL; ENDOTHELIUM CELL; ENZYMOLOGY; HUMAN; METABOLISM; PHOSPHORYLATION; VASCULAR ENDOTHELIUM;

ANIMALS; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PHOSPHOTRANSFERASES;

EID: 84899463890     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-014-1812-1     Document Type: Review

References (113)

1. Adam AP, Sharenko AL, Pumiglia K, Vincent PA (2010) SRC-induced tyrosine phosphorylation of VE-cadherin is not sufficient to decrease barrier function of endothelial monolayers. J Biol Chem 285:7045-7055
2. Alcaide P, Newton G, Auerbach S, Sehrawat S, Mayadas TN, Golan DE, Yacono P, Vincent P, Kowalczyk A, Luscinskas FW (2008) p120-catenin regulates leukocyte transmigration through an effect on VE-cadherin phosphorylation. Blood 112:2770-2779
3. Allingham MJ, van Buul JD, Burridge K (2007) ICAM-1-mediated, Src- and Pyk2-dependentvascular endothelial cadherin tyrosine phosphorylation is required for leukocyte transendothelial migration. J Immunol 179:4053-4064
4. Alonso A, Sasin J, Bottini N, Friedberg I, Osterman A, Godzik A, Hunter T, Dixon J, Mustelin T (2004) Protein tyrosine phosphatases in the human genome. Cell 117:699-711
5. Andriopoulou P, Navarro P, Zanetti A, Lampugnani MG, Dejana E (1999) Histamine induces tyrosine phosphorylation of endothelial cell-to-cell adherens junctions. Arterioscler Thromb Vasc Biol 19:2286-2297
6. Angelini DJ, Hyun S-W, Grigoryev DN, Garg P, Gong P, Singh IS, Jeffery AP, Hasday D, Goldblum SE (2006) TNF-alpha increases tyrosine phosphorylation of vascular endothelial cadherin and opens the paracellular pathway through fyn activation in human lung endothelia. Am J Physiol Lung Cell Mol Physiol 291:L1232-L1245
7. Aricescu AR, McKinnell IW, Halfter W, Stoker AW (2002) Heparan sulfate proteoglycans are ligands for receptor protein tyrosine phosphatase sigma. Mol Cell Biol 22:1881-1892
8. Balsamo J, Leung T, Ernst H, Zanin MK, Hoffman S, Lilien J (1996) Regulated binding of PTP1B-like phosphatase to N-cadherin: control of cadherin-mediated adhesion by dephosphorylation of beta-catenin. J Cell Biol 134:801-813
9. Balsamo J, Arregui C, Leung T, Lilien J (1998) The nonreceptor protein tyrosine phosphatase PTP1B binds to the cytoplasmic domain of N-cadherin and regulates the cadherin-actin linkage. J Cell Biol 143:523-532
10. Baumeister U, Funke R, Ebnet K, Vorschmitt H, Koch S, Vestweber D (2005) Association of Csk to VE-cadherin and inhibition of cell proliferation. EMBO J 24:1686-1695
11. Baumer S, Keller L, Holtmann A, Funke R, August B, Gamp A, Wolburg H, Wolburg-Buchholz K, Deutsch U, Vestweber D (2006) Vascular endothelial cell specific phospho-tyrosine phosphatase (VE-PTP) activity is required for blood vessel development. Blood 107:4754-4762
12. Belvitch P, Dudek SM (2012) Role of FAK in S1P-regulated endothelial permeability. Microvasc Res 83:22-30
13. Bixel G, Kloep S, Butz S, Petri B, Engelhardt B, Vestweber D (2004) Mouse CD99 participates in T cell recruitment into inflamed skin. Blood 104:3205-3213
14. Bixel MG, Petri B, Khandoga AG, Khandoga A, Wolburg-Buchholz K, Wolburg H, Marz S, Krombach F, Vestweber D (2007) A CD99-related antigen on endothelial cells mediates neutrophil but not lymphocyte extravasation in vivo. Blood 109:5327-5336
15. Bradfield PF, Nourshargh S, Aurrand-Lions M, Imhof BA (2007) JAM family and related proteins in leukocyte migration. Arterioscler Thromb Vasc Biol 27:2104-2112
16. Brady-Kalnay SM, Flint AJ, Tonks NK (1993) Homophilic binding of PTP mu, a receptor-type protein tyrosine phosphatase, can mediate cell-cell aggregation. J Cell Biol 122:961-972
17. Brady-Kalnay SM, Rimm DL, Tonks NK (1995) Receptor protein tyrosine phosphatase PTPmu associates with cadherins and catenins in vivo. J Cell Biol 130:977-986
18. Brady-Kalnay SM, Mourton T, Nixon JP, Pietz GE, Kinch M, Chen H, Brackenbury R, Rimm DL, Del Vecchio RL, Tonks NK (1998) Dynamic interaction of PTPmu with multiple cadherins in vivo. J Cell Biol 141:287-296
19. Broermann A, Winderlich M, Block H, Frye M, Rossaint J, Zarbock A, Cagna G, Linnepe R, Schulte D, Nottebaum AF, Vestweber D (2011) Dissociation of VE-PTP from VE-cadherin is required for leukocyte extravasation and for VEGF-induced vascular permeability in vivo. J Exp Med 208:2393-2401
20. Burks J, Agazie YM (2006) Modulation of alpha-catenin Tyr phosphorylation by SHP2 positively effects cell transformation induced by the constitutively active FGFR3. Oncogene 114
21. Campan M, Yoshizumi M, Seidah NG, Lee ME, Bianchi C, Haber E (1996) Increased proteolytic processing of protein tyrosine phosphatase mu in confluent vascular endothelial cells: the role of PC5, a member of the subtilisin family. Biochemistry 35:3797-3802
22. Cao MY, Huber M, Beauchemin N, Famiglietti J, Albelda SM, Veillette A (1998) Regulation of mouse PECAM-1 tyrosine phosphorylation by the Src and Csk families of protein-tyrosine kinases. J Biol Chem 273:15765-15772
23. Carman CV, Springer TA (2004) A transmigratory cup in leukocyte diapedesis both through individual vascular endothelial cells and between them. J Cell Biol 167:377-388
24. Carmeliet P, Lampugnani M-G, Moons L, Breviario F, Compernolle V, Bono F, Balconi G, Spagnuolo R, Oosthuyse B, Dewerchin M, Zanetti A, Angellilo A, Mattot V, Nuyens D, Lutgens E, Clotman F, de Ruiter MC, Gittenberger-de Groot A, Poelmann R, Lupu F, Herbert J-M, Collen D, Dejana E (1999) Targeted Deficiency or Cytosolic Truncation of the VE-cadherin Gene in Mice Impairs VEGF-Mediated Endothelial Survival and Angiogenesis. Cell 98:147-157
25. Carra S, Foglia E, Cermenati S, Bresciani E, Giampietro C, Lora Lamia C, Dejana E, Beltrame M, Cotelli F (2012) Ve-ptp modulates vascular integrity by promoting adherens junction maturation. PLoS One 7:e51245
26. Charbonneau H, Tonks NK, Kumar S, Diltz CD, Harrylock M, Cool DE, Krebs EG, Fischer EH, Walsh KA (1989) Human placenta protein-tyrosine-phosphatase: amino acid sequence and relationship to a family of receptor-like proteins. Proc Natl Acad Sci USA 86:5252-5256
27. Chen XL, Nam JO, Jean C, Lawson C, Walsh CT, Goka E, Lim ST, Tomar A, Tancioni I, Uryu S, Guan JL, Acevedo LM, Weis SM, Cheresh DA, Schlaepfer DD (2012) VEGF-induced vascular permeability is mediated by FAK. Dev Cell 22:146-157
28. Corada M, Mariotti M, Thurston G, Smith K, Kunkel R, Brockhaus M, Lampugnani MG, Martin-Padura I, Stoppacciaro A, Ruco L, McDonald DM, Ward PA, Dejana E (1999) Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo. Proc Natl Acad Sci USA 96:9815-9820
29. David S, Park JK, Meurs M, Zijlstra JG, Koenecke C, Schrimpf C, Shushakova N, Gueler F, Haller H, Kumpers P (2011) Acute administration of recombinant Angiopoietin-1 ameliorates multiple-organ dysfunction syndrome and improves survival in murine sepsis. Cytokine 55:251-259
30. Dejana E, Vestweber D (2013) The Role of VE-cadherin in Vascular Morphogenesis and Permeability Control. In: Roy Fv (ed) The Molecular Biology of cadherins, Elsevier, Amsterdam, (in press)
31. Dejana E, Orsenigo F, Lampugnani MG (2008) The role of adherens junctions and VE-cadheri in the control of vascular permeability. J Cell Sci 121:2115-2122
32. Detmar M, Brown LF, Schon MP, Elicker BM, Velasco P, Richard L, Fukumura D, Monsky W, Claffey KP, Jain RK (1998) Increased microvascular density and enhanced leukocyte rolling and adhesion in the skin of VEGF transgenic mice. J Invest Dermatol 111:1-6
33. Dominguez MG, Hughes VC, Pan L, Simmons M, Daly C, Anderson K, Noguera-Troise I, Murphy AJ, Valenzuela DM, Davis S, Thurston G, Yancopoulos GD, Gale NW (2007) Vascular endothelial tyrosine phosphatase (VE-PTP)-null mice undergo vasculogenesis but die embryonically because of defects in angiogenesis. Proc Natl Acad Sci USA 104:3243-3248
34. Eliceiri BP, Paul R, Schwartzberg PL, Hood JD, Leng J, Cheresh DA (1999) Selective requirement for Src kinases during VEGF-induced angiogenesis and vascular permeability. Mol Cell 4:915-924
35. Esser S, Lampugnani MG, Corada M, Dejana E, Risau W (1998) Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. J Cell Sci 111(Pt 13):1853-1865
36. Fachinger G, Deutsch U, Risau W (1999) Functional interaction of vascular endothelial-protein tyrosine phosphatase with the angiopoietin receptor Tie-2. Oncogene 18:5948-5953
37. Feng D, Nagy JA, Pyne K, Dvorak HF, Dvorak AM (1998) Neutrophils emigrate from venules by a transendothelial cell pathway in response to FMLP. J Exp Med 187:903-915
38. Furuse M, Hirase T, Itoh M, Nagafuchi A, Yonemura S, Tsukita S, Tsukita S (1993) Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol 123:1777-1788
39. Furuse M, Sasaki H, Fujimoto K, Tsukita S (1998) A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts. J Cell Biol 143:391-401
40. Gaits F, Li RY, Ragab A, Ragab Thomas JM, Chap H (1995) Increase in receptor-like protein tyrosine phosphatase activity and expression level on density-dependent growth arrest of endothelial cells. Biochem J 311:97-103
41. Gamble JR, Drew J, Trezise L, Underwood A, Parsons M, Kasminkas L, Rudge J, Yancopoulos G, Vadas MA (2000) Angiopoietin-1 is an antipermeability and anti-inflammatory agent in vitro and targets cell junctions. Circ Res 87:603-607
42. Gavard J, Gutkind JS (2006) VEGF controls endothelial-cell permeability by promoting the β arrestin-dependent endocytosis of VE-cadherin. Nat Cell Biol 8:1223-1234
43. Gebbink MF, Zondag GC, Wubbolts RW, Beijersbergen RL, van Etten I, Moolenaar WH (1993) Cell-cell adhesion mediated by a receptor-like protein tyrosine phosphatase. J Biol Chem 268:16101-16104
44. Goel S, Gupta N, Walcott BP, Snuderl M, Kesler CT, Kirkpatrick ND, Heishi T, Huang Y, Martin JD, Ager E, Samuel R, Wang S, Yazbek J, Vakoc BJ, Peterson RT, Padera TP, Duda DG, Fukumura D, Jain RK (2013) Effects of vascular-endothelial protein tyrosine phosphatase inhibition on breast cancer vasculature and metastatic progression. J Natl Cancer Inst 105(1188):1201
45. Gory-Faure S, Prandini MH, Pointu H, Roullot V, Pignot-Paintrand I, Vernet M, Huber P (1999) Role of vascular endothelial-cadherin in vascular morphogenesis. Development 126:2093-2102
46. Gotsch U, Borges E, Bosse R, Böggemeyer E, Simon M, Mossmann H, Vestweber D (1997) VE cadherin antibody accelerates neutrophil recruiment in vivo. J Cell Sci 110:583-588
47. Grinnell KL, Casserly B, Harrington EO (2009) Role of protein tyrosine phosphatase SHP2 in barrier function of pulmonary endothelium. Am J Physiol Lung Cell Mol Physiol 298:L361-L370
48. Hayashi M, Majumdar A, Li X, Adler J, Sun Z, Vertuani S, Hellberg C, Mellberg S, Koch S, Dimberg A, Koh GY, Dejana E, Belting HG, Affolter M, Thurston G, Holmgren L, Vestweber D, Claesson-Welsh L (2013) VE-PTP regulates VEGFR2 activity in stalk cells to establish endothelial cell polarity and lumen formation. Nat Commun 4:1672
49. Hudry-Clergeon H, Stengel D, Ninio E, Vilgrain I (2005) Platelet-activating factor increases VE cadherin tyrosine phosphorylation in mouse endothelial cells and its association with the PtdIns3-kinase. FASEB J 19:512-520
50. Jackson DE, Ward CM, Wang R, Newman PJ (1997) The protein-tyrosine phosphatase SHP-2 binds platelet/endothelial cell adhesion molecule-1 (PECAM-1) and forms a distinct signaling complex during platelet aggregation. Evidence for a mechanistic link between PECAM-1- and integrin-mediated cellular signaling. J Biol Chem 272:6986-6993
51. Johnson KG, Tenney AP, Ghose A, Duckworth AM, Higashi ME, Parfitt K, Marcu O, Heslip TR, Marsh JL, Schwarz TL, Flanagan JG, Van Vactor D (2006) The HSPGs Syndecan and Dallylike bind the receptor phosphatase LAR and exert distinct effects on synaptic development. Neuron 49:517-531
52. Kappert K, Peters KG, Bohmer FD, Ostman A (2005) Tyrosine phosphatases in vessel wall signaling. Cardiovasc Res 65:587-598
53. Kemler R (1993) From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion. Trends Genet 9:317-321
54. Konstantoulaki M, Kouklis P, Malik AB (2003) Protein kinase C modifications of VE-cadherin, p120, and beta-catenin contribute to endothelial barrier dysregulation induced by thrombin. Am J Physiol Lung Cell Mol Physiol 285:L434-L442
55. Kumpers P, Gueler F, David S, Slyke PV, Dumont DJ, Park JK, Bockmeyer CL, Parikh SM, Pavenstadt H, Haller H, Shushakova N (2011) The synthetic tie2 agonist peptide vasculotide protects against vascular leakage and reduces mortality in murine abdominal sepsis. Crit Care 15:R261
56. Küppers V, Vestweber D, Schulte D (2013) Locking endothelial junctions blocks leukocyte extravasation, but not in all tissues. Tissue Barriers 1:eLocation ID: e23805
57. Lampugnani MG, Zanetti A, Corada M, Takahashi T, Balconi G, Breviario F, Orsenigo F, Cattelino A, Kemler R, Daniel TO, Dejana E (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
58. Laukoetter MG, Nava P, Lee WY, Severson EA, Capaldo CT, Babbin BA, Williams IR, Koval M, Peatman E, Campbell JA, Dermody TS, Nusrat A, Parkos CA (2007) JAM-A regulates permeability and inflammation in the intestine in vivo. J Exp Med 204:3067-3076
59. Ley K, Laudanna C, Cybulsky MI, Nourshargh S (2007) Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 7:678-689
60. Lilien J, Balsamo J (2005) The regulation of cadherin-mediated adhesion by tyrosine phosphorylation/dephosphorylation of b-catenin. Curr Opin Cell Biol 17:459-465
61. Majno G, Palade GE (1961) Studies on inflammation. 1. The effect of histamine and serotonin on vascular permeability: an electron microscopic study. J Biophys Biochem Cytol 11:571-605
62. Mammoto T, Parikh SM, Mammoto A, Gallagher D, Chan B, Mostoslavsky G, Ingber DE, Sukhatme VP (2007) Angiopoietin-1 requires p190 RhoGAP to protect against vascular leakage in vivo. J Biol Chem 282:23910-23918
63. Martin-Padura I, Lostaglio S, Schneemann M, Williams L, Romano M, Fruscella P, Panzeri C, Stoppacciaro A, Ruco L, Villa A, Simmons D, Dejana E (1998) Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol 142:117-127
64. Masuda M, Osawa M, Shigematsu H, Harada N, Fujiwara K (1997) Platelet endothelial cell adhesion molecule-1 is a major SH-PTP2 binding protein in vascular endothelial cells. FEBS Lett 408:331-336
65. Mehta D, Malik AB (2006) Signaling Mechanisms regulating endothelial permeability. Physiol Rev 86:279-367
66. Mellberg S, Dimberg A, Bahram F, Hayashi M, Rennel E, Ameur A, Westholm JO, Larsson E, Lindahl P, Cross MJ, Claesson-Welsh L (2009) Transcriptional profiling reveals a critical role for tyrosine phosphatase VE-PTP in regulation of VEGFR2 activity and endothelial cell morphogenesis. FASEB J 23:1490-1502
67. Miravet S, Piedra J, Castano J, Raurell I, Franci C, Dunach M, Garcia de Herros A (2003) Tyrosine phosphorylation of plakoglobin causes contrary effects on its association with desmosomes and adherens junction components and modulates beta-catenin-mediated transcription. Mol Cell Biol 23:7391-7402
68. Monaghan-Benson E, Burridge K (2009) The regulation of vascular endothelial growth factor induced microvascular permeability requires Rac and reactive oxygen species. J Biol Chem 284:25602-25611
69. Monteiro AC, Parkos CA (2012) Intracellular mediators of JAM-A-dependent epithelial barrier function. Ann NY Acad Sci 1257:115-124
70. Morita K, Furuse M, Fujimoto K, Tsukita S (1999) Claudin multigene family encoding four transmembrane domain protein components of tight junction strands. Proc Natl Acad Sci USA 96:511-516
71. Muller WA (2011) Mechanisms of leukocyte transendothelial migration. Annu Rev Pathol 6:323-344
72. Muller WA, Weigl SA, Deng X, Phillips DM (1993) PECAM-1 is required for transendothelial migration of leukocytes. J Exp Med 178:449-460
73. Nakamura Y, Patrushev N, Inomata H, Mehta D, Urao N, Kim HW, Razvi M, Kini V, Mahadev K, Goldstein BJ, McKinney R, Fukai T, Ushio-Fukai M (2008) Role of protein tyrosine phosphatase 1B in vascular endothelial growth factor signaling and cell-cell adhesions in endothelial cells. Circ Res 102:1182-1191
74. Nawroth R, Poell G, Ranft A, Samulowitz U, Fachinger G, Golding M, Shima DT, Deutsch U, Vestweber D (2002) VE-PTP and VE-cadherin ectodomains interact to facilitate regulation of phosphorylation and cell contacts. EMBO J 21:4885-4895
75. Newman PJ, Newman DK (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
76. Nottebaum AF, Cagna G, Winderlich M, Gamp AC, Linnepe R, Polaschegg C, Filippova K, Lyck R, Engelhardt B, Kamenyeva O, Bixel MG, Butz S, Vestweber D (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
77. Okada M, Nakagawa H (1989) A protein tyrosine kinase involved in regulation of pp 60c-src function. J Biol Chem 264:20886-20893
78. Orlova VV, Economopoulou M, Lupu F, Santoso S, Chavakis T (2006) Junctional adhesion molecule-C regulates vascular endothelial permeability by modulating VE-cadherin-mediated cell-cell contacts. J Exp Med 203:2703-2714
79. Orsenigo F, Giampietro C, Ferrari A, Corada M, Galaup A, Sigismund S, Ristagno G, Maddaluno L, Young Koh G, Franco D, Kurtcuoglu V, Poulikakos D, Baluk P, McDonald D, Grazia Lampugnani M, Dejana E (2012) Phosphorylation of VE-cadherin is modulated by haemodynamic forces and contributes to the regulation of vascular permeability in vivo. Nat Commun 3:1208
80. Östman A, Yang Q, Tonks NK (1994) Expression of DEP-1, a receptor-like protein-tyrosine phosphatase, is enhanced with increasing cell density. Proc Natl Acad Sci USA 91:9680-9684
81. Piedra J, Martinez D, Castano J, Miravet S, Dunach M, de Herreros AG (2001) Regulation of beta-catenin structure and activity by tyrosine phosphorylation. J Biol Chem 276:20436-20443
82. Piedra J, Miravet S, Castano J, Palmer HG, Heisterkamp N, Garcia de Herreros A, Dunach M (2003) p120 Catenin-associated Fer and Fyn tyrosine kinases regulate beta-catenin Tyr-142 phosphorylation and beta-catenin-alpha-catenin Interaction. Mol Cell Biol 23:2287-2297
83. Saharinen P, Eklund L, Miettinen J, Wirkkala R, Anisimov A, Winderlich M, Nottebaum A, Vestweber D, Deutsch U, Koh GY, Olsen BR, Alitalo K (2008) Angiopoietins assemble distinct Tie2 signalling complexes in endothelial cell-cell and cell-matrix contacts. Nat Cell Biol 10:527-537
84. Sallee JL, Burridge K (2009) Density-enhanced phosphatase 1 regulates phosphorylation of tightjunction proteins and enhances barrier function of epithelial cells. J Biol Chem 284:14997-15006
85. Sap J, Jiang YP, Friedlander D, Grumet M, Schlessinger J (1994) Receptor tyrosine phosphatase R-PTP-kappa mediates homophilic binding. Mol Cell Biol 14:1-9
86. Schenkel AR, Mamdouh Z, Chen X, Liebman RM, Muller WA (2002) CD99 plays a major role in the migration of monocytes through endothelial junctions. Nat Immunol 3:143-150
87. Schoefl GI (1972) The migration of lymphocytes across the vascular endothelium in lymphoid tissue. A reexamination. J Exp Med 136:568-588
88. Schulte D, Küppers V, Dartsch N, Broermann A, Li H, Zarbock A, Kamenyeva O, Kiefer F, Khandoga A, Massberg S, Vestweber D (2011) Stabilizing the VE-cadherin-catenin complex blocks leukocyte extravasation and vascular permeability. EMBO J 30:4157-4170
89. Seelige R, Natsch C, März S, Jing D, Frye M, Butz S, Vestweber D (2013) Endothelial-specific gene ablation of CD99L2 impairs leukocyte extravasation in vivo. J Immunol 190:892-896
90. Sorby M, Sandstrom J, Ostman A (2001) An extracellular ligand increases the specific activity of the receptor-like protein tyrosine phosphatase DEP-1. Oncogene 20:5219-5224
91. Spring K, Chabot C, Langlois S, Lapointe L, Trinh NT, Caron C, Hebda JK, Gavard J, Elchebly M, Royal I (2012) Tyrosine phosphorylation of DEP-1/CD148 as a mechanism controlling Src kinase activation, endothelial cell permeability, invasion, and capillary formation. Blood 120:2745-2756
92. Staddon JM, Herrenknecht K, Smales C, Rubin LL (1995) Evidence that tyrosine phosphorylation may increase tight junction permeability. J Cell Sci 108(Pt 2):609-619
93. Sui XF, Kiser TD, Hyun SW, Angelini DJ, Del Vecchio RL, Young BA, Hasday JD, Romer LH, Passaniti A, Tonks NK, Goldblum SE (2005) Receptor protein tyrosine phosphatase micro regulates the paracellular pathway in human lung microvascular endothelia. Am J Pathol 166:1247-1258
94. Takahashi T, Takahashi K, St John PL, Fleming PA, Tomemori T, Watanabe T, Abrahamson DR, Drake CJ, Shirasawa T, Daniel TO (2003) A mutant receptor tyrosine phosphatase, CD148, causes defects in vascular development. Mol Cell Biol 23:1817-1831
95. Thurston G, Suri C, Smith K, McClain J, Sato TN, Yancopoulos GD, McDonald DM (1999) Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science 286:2511-2514
96. Timmerman I, Hoogenboezem M, Bennett AM, Geerts D, Hordijk PL, van Buul JD (2012) The tyrosine phosphatase SHP2 regulates recovery of endothelial adherens junctions through control of beta-catenin phosphorylation. Mol Biol Cell 23:4212-4225
97. Tonks NK, Diltz CD, Fischer EH (1988a) Characterization of the major protein-tyrosine- phosphatases of human placenta. J Biol Chem 263:6731-6737
98. Tonks NK, Diltz CD, Fischer EH (1988b) Purification of the major protein-tyrosine- phosphatases of human placenta. J Biol Chem 263:6722-6730
99. Trapasso F, Drusco A, Costinean S, Alder H, Aqeilan RI, Iuliano R, Gaudio E, Raso C, Zanesi N, Croce CM, Fusco A (2006) Genetic ablation of Ptprj, a mouse cancer susceptibility gene, results in normal growth and development and does not predispose to spontaneous tumorigenesis. DNA Cell Biol 25:376-382
100. Turowski P, Martinelli R, Crawford R, Wateridge D, Papagiorgiou A-P, Lampugnani MG, Gamp AC, Vestweber D, Adamson P, Dejana E, Greenwood J (2008) Phosphorylation of Vascular Endothelial Cadherin Controls Lymphocyte Emigration. J Cell Sci 121:29-37
101. Ukropec JA, Hollinger MK, Salva SM, Woolkalis MJ (2000) SHP2 association with VE- cadherin complexes in human endothelial cells is regulated by thrombin. J Biol Chem 275:5983-5986
102. van Buul JD, Anthony EC, Fernandez-Borja M, Burridge K, Hordijk PL (2005) Proline-rich tyrosine kinase 2 (Pyk2) mediates vascular endothelial-cadherin- based cell-cell adhesion by regulating beta-catenin tyrosine phosphorylation. J Biol Chem 280:21129-21136
103. Vestweber D (2007) Adhesion and signaling molecules controlling the transmigration of leukocytes through endothelium. Immunol Rev 218:178-196
104. Vestweber D, Winderlich M, Cagna G, Nottebaum AF (2009) Cell adhesion dynamics at endothelial junctions: VE-cadherin as a major player. Trends Cell Biol 19:8-15
105. Vockel M, Vestweber D (2013) How T cells trigger the dissociation of the endothelial receptor phosphatase VE-PTP from VE-cadherin. Blood 122:2512-2522
106. Wallez Y, Cand F, Cruzalegui F, Wernstedt C, Souchelnytskyi S, Vilgrain I, Huber P (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
107. Weber C, Fraemohs L, Dejana E (2007) The role of junctional adhesion molecules in vascular inflammation. Nat Rev Immunol 7:467-477
108. Wegmann F, Petri J, Khandoga AG, Moser C, Khandoga A, Volkery S, Li H, Nasdala I, Brandau O, Fässler R, Butz S, Krombach F, Vestweber D (2006) ESAM supports neutrophil extravasation, activation of Rho and VEGF-induced vascular permeability. J Exp Med 203:1671-1677
109. Weis S, Shintani S, Weber A, Kirchmair R, Wood M, Cravens A, McSharry H, Iwakura A, Yoon YS, Himes N, Burstein D, Doukas J, Soll R, Losordo D, Cheresh D (2004) Src blockade stabilizes a Flk/cadherin complex, reducing edema and tissue injury following myocardial infarction. J Clin Invest 113:885-894
110. Winderlich M, Keller L, Cagna G, Broermann A, Kamenyeva O, Kiefer F, Deutsch U, Nottebaum AF, Vestweber D (2009) VE-PTP controls blood vessel development by balancing Tie-2 activity. J Cell Biol 185:657-671
111. Woodfin A, Voisin MB, Beyrau M, Colom B, Caille D, Diapouli FM, Nash GB, Chavakis T, Albelda SM, Rainger GE, Meda P, Imhof BA, Nourshargh S (2011) The junctional adhesion molecule JAM-C regulates polarized transendothelial migration of neutrophils in vivo. Nat Immunol 12:761-769
112. Young BA, Sui X, Kiser TD, Hyun SW, Wang P, Sakarya S, Angelini DJ, Schaphorst KL, Hasday JD, Cross AS, Romer LH, Passaniti A, Goldblum SE (2003) Protein tyrosine phosphatase activity regulates endothelial cell-cell interactions, the paracellular pathway, and capillary tube stability. Am J Physiol Lung Cell Mol Physiol 285:L63-L75
113. Zhu JW, Brdicka T, Katsumoto TR, Lin J, Weiss A (2008) Structurally distinct phosphatases CD45 and CD148 both regulate B cell and macrophage immunoreceptor signaling. Immunity 28:183-196