VE-cadherin Y685F knock-in mouse is sensitive to vascular permeability in recurrent angiogenic organs

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 307, Issue 3, 2014, Pages

  Sidibé, Adama ^a,b,c   Polena, Helena ^a,b,c   Pernet Gallay, Karin ^d   Razanajatovo, Jeremy ^a,b,c   Mannic, Tiphaine ^a,b,c   Chaumontel, Nicolas ^a,b,c   Bama, Soumalamaya ^a,b,c   Maréchal, Irène ^a,b,c   Huber, Philippe ^a,b,c   Gulino Debrac, Danielle ^a,b,c   Bouillet, Laurence ^a,b,c,e   Vilgrain, Isabelle ^a,b,c  

^a INSERM   (France)

^b UNIV GRENOBLE ALPES   (France)

^c CEA GRENOBLE   (France)

^d GRENOBLE INSTITUT DES NEUROSCIENCES   (France)

^e GRENOBLE UNIVERSITY HOSPITAL   (France)

Author keywords

Knock in mouse; Mouse estrous cycle; Tyrosine kinase; Vascular permeability; VE cadherin phosphorylation

Indexed keywords

COLLAGEN FIBER; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN; CADHERIN; LEUKOCYTE ANTIGEN; TYROSINE;

ANIMAL EXPERIMENT; ARTICLE; BLOOD VESSEL PERMEABILITY; CAPILLARY PERMEABILITY; CELL MEMBRANE; CONTROLLED STUDY; ELECTRON MICROSCOPY; ENDOMETRIUM; ENDOTHELIUM CELL; FEMALE; MOUSE; MYOMETRIUM; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; ANGIOGENESIS; ANIMAL; C57BL MOUSE; CAPILLARY; EDEMA; GENE TARGETING; GENETICS; GENOTYPE; HOMOZYGOTE; METABOLISM; OVARY; PATHOLOGY; PATHOPHYSIOLOGY; PHENOTYPE; PHOSPHORYLATION; TRANSGENIC MOUSE; ULTRASTRUCTURE; UTERUS; VASCULARIZATION;

ANIMALS; ANTIGENS, CD; CADHERINS; CAPILLARIES; CAPILLARY PERMEABILITY; EDEMA; FEMALE; GENE KNOCK-IN TECHNIQUES; GENOTYPE; HOMOZYGOTE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOVASCULARIZATION, PHYSIOLOGIC; OVARY; PHENOTYPE; PHOSPHORYLATION; TYROSINE; UTERUS;

EID: 84905226009     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00774.2013     Document Type: Article

References (25)

1. Adam AP, Sharenko AL, Pumiglia K, Vincent PA. Src-induced tyrosine phosphorylation of VE-cadherin is not sufficient to decrease barrier function of endothelial monolayers. J Biol Chem 285: 7045-7055, 2010.
2. Allingham MJ, van Buul JD, Burridge K. ICAM-1-mediated, Src-and Pyk2-dependent vascular endothelial cadherin tyrosine phosphorylation is required for leukocyte transendothelial migration. J Immunol 179: 4053-4064, 2007.
3. Baumeister U, Funke R, Ebnet K, Vorschmitt H, Koch S, Vestweber D. Association of Csk to VE-cadherin and inhibition of cell proliferation. EMBO J 24: 1686-1695, 2005.
4. Benzinou M, Clermont FF, Letteboer TG, Kim JH, Espejel S, Harradine KA, Arbelaez J, Luu MT, Roy R, Quigley D, Higgins MN, Zaid M, Aouizerat BE, van Amstel JK, Giraud S, Dupuis-Girod S, Lesca G, Plauchu H, Hughes CC, Westermann CJ, Akhurst RJ. Mouse and human strategies identify PTPN14 as a modifier of angiogenesis and hereditary haemorrhagic telangiectasia. Nat Commun 3: 616, 2012.
5. Carmeliet P, Lampugnani MG, 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 JM, Collen D, Dejana E. Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 98: 147-157, 1999.
6. Courtneidge SA, Fumagalli S, Koegl M, Superti-Furga G, Twamley-Stein GM. The Src family of protein tyrosine kinases: regulation and functions. Dev Suppl 1993: 57-64, 1993.
7. Daniel JM, Reynolds AB. Tyrosine phosphorylation and cadherin/catenin function. Bioessays 19: 883-891, 1997.
8. Dejana E. Endothelial adherens junctions: implications in the control of vascular permeability and angiogenesis. J Clin Invest 100: S7-S10, 1997.
9. Friedl J, Puhlmann M, Bartlett DL, Libutti SK, Turner EN, Gnant MF, Alexander HR. Induction of permeability across endothelial cell monolayers by tumor necrosis factor (TNF) occurs via a tissue factordependent mechanism: relationship between the procoagulant and permeability effects of TNF. Blood 100: 1334-1339, 2002.
10. Garcia AN, Vogel SM, Komarova YA, Malik AB. Permeability of endothelial barrier: cell culture and in vivo models. Methods Mol Biol 763: 333-354, 2011.
11. Gory-Faure S, Prandini MH, Pointu H, Roullot V, Pignot-Paintrand I, Vernet M, Huber P. Role of vascular endothelial-cadherin in vascular morphogenesis. Development 126: 2093-2102, 1999.
12. Greenlee RT, Kessel B, Williams CR, Riley TL, Ragard LR, Hartge P, Buys SS, Partridge EE, Reding DJ. Prevalence, incidence, and natural history of simple ovarian cysts among women 55 years old in a large cancer screening trial. Am J Obstet Gynecol 202: 373. e371-e379, 2010.
13. Kim MP, Park SI, Kopetz S, Gallick GE. Src family kinases as mediators of endothelial permeability: effects on inflammation and metastasis. Cell Tissue Res 335: 249-259, 2009.
14. Lambeng N, Wallez Y, Rampon C, Cand F, Christe G, Gulino-Debrac D, Vilgrain I, Huber P. Vascular endothelial-cadherin tyrosine phosphorylation in angiogenic and quiescent adult tissues. Circ Res 96: 384-391, 2005.
15. Mesiano S, Ferrara N, Jaffe RB. Role of vascular endothelial growth factor in ovarian cancer: inhibition of ascites formation by immunoneutralization. Am J Pathol 153: 1249-1256, 1998.
16. Orsenigo F, Giampietro C, Ferrari A, Corada M, Galaup A, Sigismund S, Ristagno G, Maddaluno L, Koh GY, Franco D, Kurtcuoglu V, Poulikakos D, Baluk P, McDonald D, Grazia Lampugnani M, Dejana E. Phosphorylation of VE-cadherin is modulated by haemodynamic forces and contributes to the regulation of vascular permeability in vivo. Nat Commun 3: 1208, 2012.
17. 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 280: 31906-31912, 2005.
18. Sidibé A, Imhof BA. VE-cadherin phosphorylation decides: vascular permeability or diapedesis. Nat Immunol 15: 215-217, 2014.
19. Sidibé A, Polena H, Razanajatovo J, Mannic T, Chaumontel N, Bama S, Maréchal I, Huber P, Gulino-Debrac D, Bouillet L, Vilgrain I. Dynamic phosphorylation of VE-cadherin Y685 throughout mouse estrous cycle in ovary and uterus. Am J Physiol Heart Circ Physiol 307, 2014. First published May 23, 2018; doi: 10. 1152/ajpheart. 00773. 2013.
20. Taddei I, Morishima M, Huynh T, Lindsay EA. Genetic factors are major determinants of phenotypic variability in a mouse model of the DiGeorge/del22q11 syndromes. Proc Natl Acad Sci USA 98: 11428-11431, 2001.
21. Turowski P, Martinelli R, Crawford R, Wateridge D, Papageorgiou AP, Lampugnani MG, Gamp AC, Vestweber D, Adamson P, Dejana E, Greenwood J. Phosphorylation of vascular endothelial cadherin controls lymphocyte emigration. J Cell Sci 121: 29-37, 2008.
22. Vittet D, Buchou T, Schweitzer A, Dejana E, Huber P. Targeted null-mutation in the vascular endothelial-cadherin gene impairs the organization of vascular-like structures in embryoid bodies. Proc Natl Acad Sci USA 94: 6273-6278, 1997.
23. Wallez Y, Cand F, Cruzalegui F, Wernstedt C, Souchelnytskyi S, Vilgrain I, Huber P. Src kinase phosphorylates vascular endothelialcadherin in response to vascular endothelial growth factor: identification of tyrosine 685 as the unique target site. Oncogene 26: 1067-1077, 2007.
24. 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. Src blockade stabilizes a Flk/cadherin complex, reducing edema and tissue injury following myocardial infarction. J Clin Invest 113: 885-894, 2004.
25. Wessel F, Winderlich M, Holm M, Frye M, Rivera-Galdos R, Vockel M, Linnepe R, Ipe U, Stadtmann A, Zarbock A, Nottebaum AF, Vestweber D. Leukocyte extravasation and vascular permeability are each controlled in vivo by different tyrosine residues of VE-cadherin. Nat Immunol 15: 223-230, 2014.