Interfering with VE-PTP stabilizes endothelial junctions in vivo via Tie-2 in the absence of VE-cadherin

Journal of Experimental Medicine

Volumn 212, Issue 13, 2015, Pages 2267-2287

  Frye, Maike ^a   Dierkes, Martina ^a   Küppers, Verena ^a   Vockel, Matthias ^a   Tomm, Janina ^a   Zeuschner, Dagmar ^a   Rossaint, Jan ^c   Zarbock, Alexander ^c   Koh, Gou Young ^d,e   Peters, Kevin ^b   Nottebaum, Astrid Fee ^a   Vestweber, Dietmar ^a  

^a MAX PLANCK INSTITUTE FOR MOLECULAR BIOMEDICINE   (Germany)

^b Aerpio Therapeutics Inc   (United States)

^c UNIVERSITY OF MÜNSTER   (Germany)

^d Institute for Basic Science   (South Korea)

^e Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

AKB 9778; ANGIOPOIETIN RECEPTOR; F ACTIN; INTERCELLULAR ADHESION MOLECULE 1; MYOSIN II; MYOSIN LIGHT CHAIN; NERVE CELL ADHESION MOLECULE; PROTEIN TYROSINE PHOSPHATASE INHIBITOR; RAC1 PROTEIN; RAP1 PROTEIN; TAMOXIFEN; THROMBIN; UNCLASSIFIED DRUG; VASCULAR ENDOTHELIAL CADHERIN; VASCULAR ENDOTHELIAL PROTEIN TYROSINE PHOSPHATASE; VASCULOTROPIN RECEPTOR 2; AKB-9778; ANILINE DERIVATIVE; CADHERIN; COMP-ANG1 FUSION PROTEIN; HYBRID PROTEIN; LEUKOCYTE ANTIGEN; PHOSPHOTYROSINE; RECEPTOR LIKE PROTEIN TYROSINE PHOSPHATASE; SMALL INTERFERING RNA; SULFONIC ACID DERIVATIVE;

ANIMAL CELL; ARTICLE; BLOOD VESSEL PERMEABILITY; CELL CONTACT; CELL DENSITY; CELL LYSATE; CONTROLLED STUDY; ELECTRON MICROSCOPY; EMBRYO; ENDOTHELIUM; ENZYME ACTIVE SITE; ENZYME STABILITY; EXON; FEMALE; GENE EXPRESSION; GENE INACTIVATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IN VIVO STUDY; LEUKOCYTE; LUNG LAVAGE; MOUSE; NEUTROPHIL; NONHUMAN; PERMEABILITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; SOUTHERN BLOTTING; STOP CODON; STRESS FIBER; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; UMBILICAL VEIN ENDOTHELIAL CELL; ANIMAL; C57BL MOUSE; CAPILLARY PERMEABILITY; CELL MOTION; CYTOLOGY; DEFICIENCY; DRUG EFFECTS; ENDOTHELIUM CELL; GENE DELETION; GENE SILENCING; KNOCKOUT MOUSE; METABOLISM; PHOSPHORYLATION; ULTRASTRUCTURE;

ANILINE COMPOUNDS; ANIMALS; ANTIGENS, CD; CADHERINS; CAPILLARY PERMEABILITY; CELL MOVEMENT; ENDOTHELIAL CELLS; GENE DELETION; GENE SILENCING; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHILS; PHOSPHORYLATION; PHOSPHOTYROSINE; RAP1 GTP-BINDING PROTEINS; RECEPTOR, TIE-2; RECEPTOR-LIKE PROTEIN TYROSINE PHOSPHATASES, CLASS 3; RECOMBINANT FUSION PROTEINS; RNA, SMALL INTERFERING; SULFONIC ACIDS;

EID: 84961218854     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20150718     Document Type: Article

References (51)

1. Allingham, M.J., J.D. van Buul, and K. Burridge. 2007. ICAM-1-mediated, Srcand Pyk2-dependent vascular endothelial cadherin tyrosine phosphorylation is required for leukocyte transendothelial migration. J. Immunol. 179:4053-4064. http://dx.doi.org/10.4049/jimmunol.179.6.4053
2. Ando, K., S. Fukuhara, T. Moriya, Y. Obara, N. Nakahata, and N. Mochizuki. 2013. Rap1 potentiates endothelial cell junctions by spatially controlling myosin II activity and actin organization. J. Cell Biol. 202:901-916. http://dx.doi.org/10.1083/jcb.201301115
3. Bäumer, S., L. Keller, A. Holtmann, R. Funke, B. August, A. Gamp, H. Wolburg, K. Wolburg-Buchholz, U. Deutsch, and D. Vestweber. 2006. Vascular endothelial cell-specific phosphotyrosine phosphatase (VEPTP) activity is required for blood vessel development. Blood. 107:4754-4762. http://dx.doi.org/10.1182/blood-2006-01-0141
4. Brachtendorf, G., A. Kuhn, U. Samulowitz, R. Knorr, E. Gustafsson, A.J. Potocnik, R. Fässler, and D. Vestweber. 2001. Early expression of endomucin on endothelium of the mouse embryo and on putative hematopoietic clusters in the dorsal aorta. Dev. Dyn. 222:410-419. http://dx.doi.org/10.1002/dvdy.1199
5. Breviario, F., L. Caveda, M. Corada, I. Martin-Padura, P. Navarro, J. Golay, M. Introna, D. Gulino, M.G. Lampugnani, and E. Dejana. 1995. Functional properties of human vascular endothelial cadherin (7B4/cadherin-5), an endothelium-specific cadherin. Arterioscler. Thromb. Vasc. Biol. 15:1229-1239. http://dx.doi.org/10.1161/01.ATV.15.8.1229
6. Broermann, A., M. Winderlich, H. Block, M. Frye, J. Rossaint, A. Zarbock, G. Cagna, R. Linnepe, D. Schulte, A.F. Nottebaum, and D. Vestweber. 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. http://dx.doi.org/10.1084/jem.20110525
7. Claxton, S., V. Kostourou, S. Jadeja, P. Chambon, K. Hodivala-Dilke, and M. Fruttiger. 2008. Efficient, inducible Cre-recombinase activation in vascular endothelium. Genesis. 46:74-80. http://dx.doi.org/10.1002/dvg.20367
8. Corada, M., M. Mariotti, G. Thurston, K. Smith, R. Kunkel, M. Brockhaus, M.G. Lampugnani, I. Martin-Padura, A. Stoppacciaro, L. Ruco, et al. 1999. Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo. Proc. Natl. Acad. Sci. USA. 96:9815-9820. http://dx.doi.org/10.1073/pnas.96.17.9815
9. David, S., C.C. Ghosh, A. Mukherjee, and S.M. Parikh. 2011. Angiopoietin-1 requires IQ domain GTPase-activating protein 1 to activate Rac1 and promote endothelial barrier defense. Arterioscler. Thromb. Vasc. Biol. 31:2643-2652. http://dx.doi.org/10.1161/ATV BAHA.111.233189
10. Dejana, E., and D. Vestweber. 2013. The role of VE-cadherin in vascular morphogenesis and permeability control. In The Molecular Biology of Cadherins. Progress in Molecular Biology and Translational Science. Vol. 116. F. van Roy, editor. Elsevier, Oxford. 119-144. http://dx.doi.org/10.1016/B978-0-12-394311-8.00006-6
11. Dominguez, M.G., V.C. Hughes, L. Pan, M. Simmons, C. Daly, K. Anderson, I. Noguera-Troise, A.J. Murphy, D.M. Valenzuela, S. Davis, et al. 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. http://dx.doi.org/10.1073/pnas.0611510104
12. Ebnet, K., C.U. Schulz, M.-K. Meyer Zu Brickwedde, G.G. Pendl, and D. Vestweber. 2000. Junctional adhesion molecule interacts with the PDZ domain-containing proteins AF-6 and ZO-1. J. Biol. Chem. 275:27979-27988.
13. Fachinger, G., U. Deutsch, and W. Risau. 1999. Functional interaction of vascular endothelial-protein-tyrosine phosphatase with the angiopoietin receptor Tie-2. Oncogene. 18:5948-5953. http://dx.doi.org/10.1038/sj.onc.1202992
14. Fukuhara, S., A. Sakurai, H. Sano, A. Yamagishi, S. Somekawa, N. Takakura, Y. Saito, K. Kangawa, and N. Mochizuki. 2005. Cyclic AMP potentiates vascular endothelial cadherin-mediated cell-cell contact to enhance endothelial barrier function through an Epac-Rap1 signaling pathway. Mol. Cell. Biol. 25:136-146. http://dx.doi.org/10.1128/MCB.25.1.136-146.2005
15. Fukuhara, S., K. Sako, T. Minami, K. Noda, H.Z. Kim, T. Kodama, M. Shibuya, N. Takakura, G.Y. Koh, and 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. http://dx.doi.org/10.1038/ncb1714
16. Gamble, J.R., J. Drew, L. Trezise, A. Underwood, M. Parsons, L. Kasminkas, J. Rudge, G. Yancopoulos, and M.A. Vadas. 2000. Angiopoietin-1 is an antipermeability and anti-inflammatory agent in vitro and targets cell junctions. Circ. Res. 87:603-607. http://dx.doi.org/10.1161/01.RES.87.7.603
17. Gavard, J., V. Patel, and J.S. Gutkind. 2008. Angiopoietin-1 prevents VEGFinduced endothelial permeability by sequestering Src through mDia. Dev. Cell. 14:25-36. http://dx.doi.org/10.1016/j.devcel.2007.10.019
18. Giampietro, C., A. Taddei, M. Corada, G.M. Sarra-Ferraris, M. Alcalay, U. Cavallaro, F. Orsenigo, M.G. Lampugnani, and E. Dejana. 2012. Overlapping and divergent signaling pathways of N-cadherin and VEcadherin in endothelial cells. Blood. 119:2159-2170. http://dx.doi.org/10.1182/blood-2011-09-381012
19. Goel, S., N. Gupta, B.P. Walcott, M. Snuderl, C.T. Kesler, N.D. Kirkpatrick, T. Heishi, Y. Huang, J.D. Martin, E. Ager, et al. 2013. Effects of vascularendothelial protein tyrosine phosphatase inhibition on breast cancer vasculature and metastatic progression. J. Natl. Cancer Inst. 105:1188-1201. http://dx.doi.org/10.1093/jnci/djt164
20. Gong, H., J. Rehman, H. Tang, K. Wary, M. Mittal, P. Chaturvedi, Y.Y. Zhao, Y.A. Komarova, S.M. Vogel, and A.B. Malik. 2015. HIF2α signaling inhibits adherens junctional disruption in acute lung injury. J. Clin. Invest. 125:652-664. (published erratum appears in J. Clin. Invest. 2015. 125:1364) http://dx.doi.org/10.1172/JCI77701
21. Gotsch, U., E. Borges, R. Bosse, E. Böggemeyer, M. Simon, H. Mossmann, and D. Vestweber. 1997. VE-cadherin antibody accelerates neutrophil recruitment in vivo. J. Cell Sci. 110:583-588.
22. Hakanpaa, L., T. Sipila, V.M. Leppanen, P. Gautam, H. Nurmi, G. Jacquemet, L. Eklund, J. Ivaska, K. Alitalo, and P. Saharinen. 2015. Endothelial destabilization by angiopoietin-2 via integrin β1 activation. Nat. Commun. 6:5962. http://dx.doi.org/10.1038/ncomms6962
23. Hayashi, M., A. Majumdar, X. Li, J. Adler, Z. Sun, S. Vertuani, C. Hellberg, S. Mellberg, S. Koch, A. Dimberg, et al. 2013. VE-PTP regulates VEG FR2 activity in stalk cells to establish endothelial cell polarity and lumen formation. Nat. Commun. 4:1672. http://dx.doi.org/10.1038/ncomms2683
24. Koblizek, T.I., A.S. Runting, S.A. Stacker, A.F. Wilks, W. Risau, and U. Deutsch. 1997. Tie2 receptor expression and phosphorylation in cultured cells and mouse tissues. Eur. J. Biochem. 244:774-779. http://dx.doi.org/10.1111/j.1432-1033.1997.00774.x
25. Kooistra, M.R., M. Corada, E. Dejana, and J.L. Bos. 2005. Epac1 regulates integrity of endothelial cell junctions through VE-cadherin. FEBS Lett. 579:4966-4972. http://dx.doi.org/10.1016/j.febslet.2005.07.080
26. Lallemand, Y., V. Luria, R. Haffner-Krausz, and P. Lonai. 1998. Maternally expressed PGK-Cre transgene as a tool for early and uniform activation of the Cre site-specific recombinase. Transgenic Res. 7:105-112. http://dx.doi.org/10.1023/A :1008868325009
27. Mamluk, R., M. Klagsbrun, M. Detmar, and D.R. Bielenberg. 2005. Soluble neuropilin targeted to the skin inhibits vascular permeability. Angiogenesis. 8:217-227. http://dx.doi.org/10.1007/s10456-005-9009-6
28. Mammoto, T., S.M. Parikh, A. Mammoto, D. Gallagher, B. Chan, G. Mostoslavsky, D.E. Ingber, and V.P. Sukhatme. 2007. Angiopoietin-1 requires p190 RhoGAP to protect against vascular leakage in vivo. J. Biol. Chem. 282:23910-23918. http://dx.doi.org/10.1074/jbc.M702169200
29. Mellberg, S., A. Dimberg, F. Bahram, M. Hayashi, E. Rennel, A. Ameur, J.O. Westholm, E. Larsson, P. Lindahl, M.J. Cross, and L. Claesson-Welsh. 2009. Transcriptional profiling reveals a critical role for tyrosine phosphatase VE-PTP in regulation of VEG FR2 activity and endothelial cell morphogenesis. FAS EB J. 23:1490-1502. http://dx.doi.org/10.1096/fj.08-123810
30. Mochizuki, N. 2009. Vascular integrity mediated by vascular endothelial cadherin and regulated by sphingosine 1-phosphate and angiopoietin-1. Circ. J. 73:2183-2191. http://dx.doi.org/10.1253/circj.CJ-09-0666
31. Monaghan-Benson, E., and K. Burridge. 2009. The regulation of vascular endothelial growth factor-induced microvascular permeability requires Rac and reactive oxygen species. J. Biol. Chem. 284:25602-25611. http://dx.doi.org/10.1074/jbc.M109.009894
32. Morgan, S.M., U. Samulowitz, L. Darley, D.L. Simmons, and D. Vestweber. 1999. Biochemical characterization and molecular cloning of a novel endothelial-specific sialomucin. Blood. 93:165-175.
33. Nawroth, R., G. Poell, A. Ranft, S. Kloep, U. Samulowitz, G. Fachinger, M. Golding, D.T. Shima, U. Deutsch, and D. Vestweber. 2002. VEPTP and VE-cadherin ectodomains interact to facilitate regulation of phosphorylation and cell contacts. EMBO J. 21:4885-4895. http://dx.doi.org/10.1093/emboj/cdf497
34. Ngok, S.P., R. Geyer, M. Liu, A. Kourtidis, S. Agrawal, C. Wu, H.R. Seerapu, L.J. Lewis-Tuffin, K.L. Moodie, D. Huveldt, et al. 2012. VEGF and Angiopoietin-1 exert opposing effects on cell junctions by regulating the Rho GEF Syx. J. Cell Biol. 199:1103-1115. http://dx.doi.org/10.1083/jcb.201207009
35. Nitta, T., M. Hata, S. Gotoh, Y. Seo, H. Sasaki, N. Hashimoto, M. Furuse, and S. Tsukita. 2003. Size-selective loosening of the blood-brain barrier in claudin-5-deficient mice. J. Cell Biol. 161:653-660. http://dx.doi.org/10.1083/jcb.200302070
36. Nottebaum, A.F., G. Cagna, M. Winderlich, A.C. Gamp, R. Linnepe, C. Polaschegg, K. Filippova, R. Lyck, B. Engelhardt, O. Kamenyeva, et al. 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. http://dx.doi.org/10.1084/jem.20080406
37. Orsenigo, F., C. Giampietro, A. Ferrari, M. Corada, A. Galaup, S. Sigismund, G. Ristagno, L. Maddaluno, G.Y. Koh, D. Franco, et al. 2012. Phosphorylation of VE-cadherin is modulated by haemodynamic forces and contributes to the regulation of vascular permeability in vivo. Nat. Commun. 3:1208. http://dx.doi.org/10.1038/ncomms2199
38. Post, A., W.J. Pannekoek, S.H. Ross, I. Verlaan, P.M. Brouwer, and J.L. Bos. 2013. Rasip1 mediates Rap1 regulation of Rho in endothelial barrier function through ArhGAP29. Proc. Natl. Acad. Sci. USA. 110:11427-11432. http://dx.doi.org/10.1073/pnas.1306595110
39. Saharinen, P., L. Eklund, J. Miettinen, R. Wirkkala, A. Anisimov, M. Winderlich, A. Nottebaum, D. Vestweber, U. Deutsch, G.Y. Koh, et al. 2008. Angiopoietins assemble distinct Tie2 signalling complexes in endothelial cell-cell and cell-matrix contacts. Nat. Cell Biol. 10:527-537. http://dx.doi.org/10.1038/ncb1715
40. Sakuraba, J., T. Shintani, S. Tani, and M. Noda. 2013. Substrate specificity of R3 receptor-like protein-tyrosine phosphatase subfamily toward receptor protein-tyrosine kinases. J. Biol. Chem. 288:23421-23431. http://dx.doi.org/10.1074/jbc.M113.458489
41. Schulte, D., V. Küppers, N. Dartsch, A. Broermann, H. Li, A. Zarbock, O. Kamenyeva, F. Kiefer, A. Khandoga, S. Massberg, and D. Vestweber. 2011. Stabilizing the VE-cadherin-catenin complex blocks leukocyte extravasation and vascular permeability. EMBO J. 30:4157-4170. http://dx.doi.org/10.1038/emboj.2011.304
42. Shen, J., M. Frye, B.L. Lee, J.L. Reinardy, J.M. McClung, K. Ding, M. Kojima, H. Xia, C. Seidel, R. Lima e Silva, et al. 2014. Targeting VE-PTP activates TIE2 and stabilizes the ocular vasculature. J. Clin. Invest. 124:4564-4576. http://dx.doi.org/10.1172/JCI74527
43. Taddei, A., C. Giampietro, A. Conti, F. Orsenigo, F. Breviario, V. Pirazzoli, M. Potente, C. Daly, S. Dimmeler, and E. Dejana. 2008. Endothelial adherens junctions control tight junctions by VE-cadherin-mediated upregulation of claudin-5. Nat. Cell Biol. 10:923-934. http://dx.doi.org/10.1038/ncb1752
44. Thurston, G., J.S. Rudge, E. Ioffe, H. Zhou, L. Ross, S.D. Croll, N. Glazer, J. Holash, D.M. McDonald, and G.D. Yancopoulos. 2000. Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat. Med. 6:460-463. http://dx.doi.org/10.1038/74725
45. Turowski, P., R. Martinelli, R. Crawford, D. Wateridge, A.P. Papageorgiou, M.G. Lampugnani, A.C. Gamp, D. Vestweber, P. Adamson, E. Dejana, and J. Greenwood. 2008. Phosphorylation of vascular endothelial cadherin controls lymphocyte emigration. J. Cell Sci. 121:29-37. http://dx.doi.org/10.1242/jcs.022681
46. Vockel, M., and D. Vestweber. 2013. How T cells trigger the dissociation of the endothelial receptor phosphatase VE-PTP from VE-cadherin. Blood. 122:2512-2522. http://dx.doi.org/10.1182/blood-2013-04-499228
47. Wang, Y., M. Nakayama, M.E. Pitulescu, T.S. Schmidt, M.L. Bochenek, A. Sakakibara, S. Adams, A. Davy, U. Deutsch, U. Lüthi, et al. 2010. Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature. 465:483-486. http://dx.doi.org/10.1038/nature09002
48. Wegmann, F., B. Petri, A.G. Khandoga, C. Moser, A. Khandoga, S. Volkery, H. Li, I. Nasdala, O. Brandau, R. Fässler, et al. 2006. ESAM supports neutrophil extravasation, activation of Rho, and VEGF-induced vascular permeability. J. Exp. Med. 203:1671-1677. http://dx.doi.org/10.1084/jem.20060565
49. Wessel, F., M. Winderlich, M. Holm, M. Frye, R. Rivera-Galdos, M. Vockel, R. Linnepe, U. Ipe, A. Stadtmann, A. Zarbock, et al. 2014. Leukocyte extravasation and vascular permeability are each controlled in vivo by different tyrosine residues of VE-cadherin. Nat. Immunol. 15:223-230. http://dx.doi.org/10.1038/ni.2824
50. Winderlich, M., L. Keller, G. Cagna, A. Broermann, O. Kamenyeva, F. Kiefer, U. Deutsch, A.F. Nottebaum, and D. Vestweber. 2009. VE-PTP controls blood vessel development by balancing Tie-2 activity. J. Cell Biol. 185:657-671. http://dx.doi.org/10.1083/jcb.200811159
51. Zarbock, A., M.R. Distasi, E. Smith, J.M. Sanders, G. Kronke, B.L. Harry, S. von Vietinghoff, K. Buscher, J.L. Nadler, and K. Ley. 2009. Improved survival and reduced vascular permeability by eliminating or blocking 12/15-lipoxygenase in mouse models of acute lung injury (ALI). J. Immunol. 183:4715-4722. http://dx.doi.org/10.4049/jimmunol.0802592