IQGAP1 mediates VE-cadherin-based cell-cell contacts and VEGF signaling at adherence junctions linked to angiogenesis

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 26, Issue 9, 2006, Pages 1991-1997

  Yamaoka Tojo, Minako ^a   Tojo, Taiki ^a   Kim, Ha Won ^a   Hilenski, Lula ^a   Patrushev, Nikolay A ^a   Zhang, Lynn ^a   Fukai, Tohru ^a   Ushio Fukai, Masuko ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; Cell cell adherions; IQGAP1; Reactive oxygen species; Vascular endothelial growth factor; VE cadherin

Indexed keywords

ACTIN; BETA CATENIN; IQ MOTIF CONTAINING GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN 1; REACTIVE OXYGEN METABOLITE; VASCULAR ENDOTHELIAL CADHERIN; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ARTICLE; CAPILLARY PROLIFERATION; CELL CONTACT; CELL JUNCTION; CELL MOTILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENDOTHELIUM CELL; HINDLIMB; HUMAN; HUMAN CELL; LIMB ISCHEMIA; MORPHOGENESIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; VASCULAR ENDOTHELIUM;

ADHERENS JUNCTIONS; ANIMALS; ANTIGENS, CD; BETA CATENIN; CADHERINS; CELL COMMUNICATION; CELLS, CULTURED; HINDLIMB; HUMANS; ISCHEMIA; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHORYLATION; RAS GTPASE-ACTIVATING PROTEINS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SUBCELLULAR FRACTIONS; TISSUE DISTRIBUTION; TYROSINE; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 33747423658     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.0000231524.14873.e7     Document Type: Article

References (31)

1. Matsumoto T, Claesson-Welsh L. VEGF receptor signal transduction. Sci STKE. 2001;2001:RE21.
2. Ausprunk DH, Folkman J. Migration and proliferation of endothelial cells in preformed and newly formed blood vessels during tumor angiogenesis. Microvasc Res. 1977;14:53-65.
3. Dejana E, Corada M, Lampugnani MG. Endothelial cell-to-cell junctions. Faseb J. 1995;9:910-918.
4. Carmeliet P, Lampugnani MG, Moons L, Breviario F, Compernolle V, Bono F, Balconi G, Spagnuolo R, Oostuyse 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. 1999;98:147-157.
5. Esser S, Lampugnani MG, Corada M, Dejana E, Risau W. Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. J Cell Sci. 1998;111(Pt 13):1853-1865.
6. Wright TJ, Leach L, Shaw PE, Jones P. Dynamics of vascular endothelial-cadherin and beta-catenin localization by vascular endothelial growth factor-induced angiogenesis in human umbilical vein cells. Exp Cell Res. 2002;280:159-168.
7. Nawroth R, Poell G, Ranft A, Kloep S, Samulowitz U, Fachinger G, Golding M, Shima DT, Deutsch U, Vestweber D. VE-PTP and VE-cadherin ectodomains interact to facilitate regulation of phosphorylation and cell contacts. EMBO J. 2002;21:4885-4895.
8. van Wetering S, van Buul JD, Quik S, Mul FP, Anthony EC, ten Klooster JP, Collard JG, Hordijk PL. Reactive oxygen species mediate Rac-induced loss of cell-cell adhesion in primary human endothelial cells. J Cell Sci. 2002;115:1837-1846.
9. Lin MT, Yen ML, Lin CY, Kuo ML. Inhibition of vascular endothelial growth factor-induced angiogenesis by resveratrol through interruption of Src-dependent vascular endothelial cadherin tyrosine phosphorylation. Mol Pharmacol. 2003;64:1029-1036.
10. Ushio-Fukai M, Tang Y, Fukai T, Dikalov S, Ma Y, Fujimoto M, Quinn MT, Pagano PJ, Johnson C, Alexander RW. Novel role of gp91phox-containing NAD(P)H oxidase in vascular endothelial growth factor-induced signaling and angiogenesis. Circ Res. 2002;91:1160-1167.
11. Tojo T, Ushio-Fukai M, Yamaoka-Tojo M, Ikeda S, Patrushev NA, Alexander RW. Role of gp91phox (Nox2)-containing NAD(P)H oxidase in angiogenesis in response to hindlimb ischemia. Circulation. 2005;111:2347-2355.
12. Yamaoka-Tojo M, Ushio-Fukai M, Hilenski L, Dikalov SI, Chen YE, Tojo T, Fukai T, Fujimoto M, Patrushev NA, Wang N, Kontos CD, Bloom GS, Alexander RW. IQGAP1, a novel vascular endothelial growth factor receptor binding protein, is involved in reactive oxygen species-dependent endothelial migration and proliferation. Circ Res. 2004;95: 276-283.
13. Mateer SC, Wang N, Bloom GS. IQGAPs: integrators of the cytoskeleton, cell adhesion machinery, and signaling networks. Cell Motil Cytoskeleton. 2003;55:147-155.
14. Briggs MW, Sacks DB. IQGAP proteins are integral components of cytoskeletal regulation. EMBO Rep. 2003;4:571-574.
15. Noritake J, Watanabe T, Sato K, Wang S, Kaibuchi K. IQGAP1: a key regulator of adhesion and migration. J Cell Sci. 2005;118:2085-2092.
16. Hart MJ, Callow MG, Souza B, Polakis P. IQGAP1, a calmodulin-binding protein with a rasGAP-related domain, is a potential effector for cdc42Hs. EMBO J. 1996;15:2997-3005.
17. Kuroda S, Fukata M, Kobayashi K, Nakafuku M, Nomura N, Iwamatsu A, Kaibuchi K. Identification of IQGAP as a putative target for the small GTPases, Cdc42 and Rac1. J Biol Chem. 1996;271:23363-23367.
18. Mataraza JM, Briggs MW, Li Z, Entwistle A, Ridley AJ, Sacks DB. IQGAP1 promotes cell motility and invasion. J Biol Chem. 2003;278:41237-41245.
19. Kuroda S, Fukata M, Nakagawa M, Fujii K, Nakamura T, Ookubo T, Izawa I, Nagase T, Nomura N, Tani H, Shoji I, Matsuura Y, Yonehara S, Kaibuchi K. Role of IQGAP1, a target of the small GTPases Cdc42 and Rac1, in regulation of E-cadherin- mediated cell-cell adhesion. Science. 1998;281:832-835.
20. Noritake J, Fukata M, Sato K, Nakagawa M, Watanabe T, Izumi N, Wang S, Fukata Y, Kaibuchi K. Positive role of IQGAP1, an effector of Rac1, in actin-meshwork formation at sites of cell-cell contact. Mol Biol Cell. 2004;15:1065-1076.
21. Esser S, Wolburg K, Wolburg H, Breier G, Kurzchalia T, Risau W. Vascular endothelial growth factor induces endothelial fenestrations in vitro. J Cell Biol. 1998;140:947-959.
22. Couffinhal T, Silver M, Zheng LP, Kearney M, Witzenbichler B, Isner JM. Mouse model of angiogenesis. Am J Pathol. 1998;152:1667-1679.
23. Jacobi J, Tam BY, Wu G, Hoffman J, Cooke JP, Kuo CJ. Adenoviral gene transfer with soluble vascular endothelial growth factor receptors impairs angiogenesis and perfusion in a murine model of hindlimb ischemia. Circulation. 2004;110:2424-2429.
24. Ikeda S, Yamaoka-Tojo M, Hilenski L, Patrushev NA, Anwar GM, Quinn MT, Ushio-Fukai M. IQGAP1 regulates reactive oxygen species-dependent endothelial cell migration through interacting with Nox2. Arterioscler Thromb Vasc Biol. 2005;25:2295-2300.
25. Lim MJ, Chiang ET, Hechtman HB, Shepro D. Inflammation-induced subcellular redistribution of VE-cadherin, actin, and gamma-catenin in cultured human lung microvessel endothelial cells. Microvasc Res. 2001;62:366-382.
26. Alexander JS, Alexander BC, Eppihimer LA, Goodyear N, Haque R, Davis CP, Kalogeris TJ, Carden DL, Zhu YN, Kevil CG. Inflammatory mediators induce sequestration of VE-cadherin in cultured human endothelial cells. Inflammation. 2000;24:99-113.
27. Ukropec JA, Hollinger MK, Woolkalis MJ. Regulation of VE-cadherin linkage to the cytoskeleton in endothelial cells exposed to fluid shear stress. Exp Cell Res. 2002;273:240-247.
28. Rhee SG, Bae YS, Lee SR, Kwon J. Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation. Sci STKE. 2000;PE1.
29. Finkel T. Signal transduction by reactive oxygen species in non-phagocytic cells. J Leukoc Biol. 1999;65:337-430.
30. Chiarugi P, Cirri P. Redox regulation of protein tyrosine phosphatases during receptor tyrosine kinase signal transduction. Trends Biochem Sci. 2003;28:509-514.
31. Ukropec JA, Hollinger MK, Salva SM, Woolkalis MJ. SHP2 association with VE-cadherin complexes in human endothelial cells is regulated by thrombin. J Biol Chem. 2000;275:5983-5986.