Role of afadin in vascular endothelial growth factor-and sphingosine 1-phosphate-induced angiogenesis

Circulation Research

Volumn 106, Issue 11, 2010, Pages 1731-1742

  Tawa, Hideto ^a   Rikitake, Yoshiyuki ^a   Takahashi, Motonori ^a,b   Amano, Hisayuki ^a   Miyata, Muneaki ^a   Satomi Kobayashi, Seimi ^a,b   Kinugasa, Mitsuo ^a,b   Nagamatsu, Yuichi ^a   Majima, Takashi ^a   Ogita, Hisakazu ^a   Miyoshi, Jun ^b   Hirata, Ken Ichi ^a   Takai, Yoshimi ^a  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OSAKA MEDICAL CENTER FOR CANCER AND CARDIOVASCULAR DISEASES   (Japan)

Author keywords

Adhesion molecule; Apoptosis; Knockout mice; Migration; Proliferation

Indexed keywords

AFADIN; GAP JUNCTION PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RAP1 PROTEIN; SMALL INTERFERING RNA; SPHINGOSINE 1 PHOSPHATE; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANGIOGENESIS; APOPTOSIS; ARTICLE; CELL CONTACT; CELL MIGRATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; UMBILICAL VEIN; VASCULAR ENDOTHELIUM;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; APOPTOSIS; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; HINDLIMB; HUMANS; INTERCELLULAR JUNCTIONS; ISCHEMIA; LYSOPHOSPHOLIPIDS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; MUSCLE, SKELETAL; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; RAC1 GTP-BINDING PROTEIN; RAP1 GTP-BINDING PROTEINS; RATS; RECOMBINANT FUSION PROTEINS; RETINAL NEOVASCULARIZATION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SPHINGOSINE; TIME FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 77953810728     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.110.216747     Document Type: Article

References (39)

1. Dejana E. Endothelial cell-cell junctions: happy together. Nat Rev Mol Cell Biol. 2004;5:261-270.
2. 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. 1999;126:2093-2102.
3. 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. Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo. Proc Natl Acad Sci USA. 1999;96:9815-9820.
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 angio-genesis. Cell. 1999;98:147-157.
5. Kawata M, Matsui Y, Kondo J, Hishida T, Teranishi Y, Takai Y. A novel small molecular weight GTP-binding protein with the same putative effector domain as the ras proteins in bovine brain membranes. Purification, determination of primary structure, and characterization. J Biol Chem. 1988;263:18965-18971.
6. Bos JL. Linking Rap to cell adhesion. Curr Opin Cell Biol. 2005;17: 123-128.
7. Fujita H, Fukuhara S, Sakurai A, Yamagishi A, Kamioka Y, Nakaoka Y, Masuda M, Mochizuki N. Local activation of Rap1 contributes to directional vascular endothelial cell migration accompanied by extension of microtubules on which RAPL, a Rap1-associating molecule, localizes. J Biol Chem. 2005;280:5022-5031.
8. Takahashi M, Rikitake Y, Nagamatsu Y, Hara T, Ikeda W, Hirata KI, Takai Y. Sequential activation of Rap1 and Rac1 small G proteins by PDGF locally at leading edges of NIH3T3 cells. Genes Cells. 2008;13: 549-569.
9. Fukuhara S, Sakurai A, Sano H, Yamagishi A, Somekawa S, Takakura N, Saito Y, Kangawa K, Mochizuki N. Cyclic AMP potentiates vascular endothelial cadherin-mediated cell-cell contact to enhance endothelial barrier function through an Epac-Rap1 signaling pathway. Mol Cell Biol. 2005;25:136-146.
10. Chrzanowska-Wodnicka M, Kraus AE, Gale D, White GC, II, Vansluys J. Defective angiogenesis, endothelial migration, proliferation, and MAPK signaling in Rap1b-deficient mice. Blood. 2008;111:2647-2656.
11. Yan J, Li F, Ingram DA, Quilliam LA. Rap1a is a key regulator of FGF2-induced angiogenesis and together with Rap1b controls human endothelial cell functions. Mol Cell Biol. 2008;28:5801-5810.
12. Carmona G, Gottig S, Orlandi A, Scheele J, Bauerle T, Jugold M, Kiessling F, Henschler R, Zeiher AM, Dimmeler S, Chavakis E. Role of the small GTPase Rap1 for integrin activity regulation in endothelial cells and angiogenesis. Blood. 2009;113:488-497.
13. Mandai K, Nakanishi H, Satoh A, Obaishi H, Wada M, Nishioka H, Itoh M, Mizoguchi A, Aoki T, Fujimoto T, Matsuda Y, Tsukita S, Takai Y. Afadin: a novel actin filament-binding protein with one PDZ domain localized at cadherin-based cell-to-cell adherens junction. J Cell Biol. 1997;139:517-528.
14. Takai Y, Ikeda W, Ogita H, Rikitake Y. The immunoglobulin-like cell adhesion molecule nectin and its associated protein afadin. Annu Rev Cell Dev Biol. 2008;24:309-342.
15. Rikitake Y, Takai Y. Interactions of the cell adhesion molecule nectin with transmembrane and peripheral membrane proteins for pleiotropic functions. Cell Mol Life Sci. 2008;65:253-263.
16. Hoshino T, Sakisaka T, Baba T, Yamada T, Kimura T, Takai Y. Regulation of E-cadherin endocytosis by nectin through afadin, Rap1, and p120ctn. J Biol Chem. 2005;280:24095-24103.
17. Sato T, Fujita N, Yamada A, Ooshio T, Okamoto R, Irie K, Takai Y. Regulation of the assembly and adhesion activity of E-cadherin by nectin and afadin for the formation of adherens junctions in Madin-Darby canine kidney cells. J Biol Chem. 2006;281:5288-5299.
18. Nakata S, Fujita N, Kitagawa Y, Okamoto R, Ogita H, Takai Y. Regulation of platelet-derived growth factor receptor activation by afadin through SHP-2: implications for cellular morphology. J Biol Chem. 2007; 282:37815-37825.
19. Miyata M, Rikitake Y, Takahashi M, Nagamatsu Y, Yamauchi Y, Ogita H, Hirata K, Takai Y. Regulation by afadin of cyclical activation and inactivation of Rap1, Rac1, and RhoA small G proteins at leading edges of moving NIH3T3 cells. J Biol Chem. 2009;284:24595-24609.
20. Linnemann T, Geyer M, Jaitner BK, Block C, Kalbitzer HR, Wittinghofer A, Herrmann C. Thermodynamic and kinetic characterization of the interaction between the Ras binding domain of AF6 and members of the Ras subfamily. J Biol Chem. 1999;274:13556-13562.
21. Boettner B, Govek EE, Cross J, Van Aelst L. The junctional multidomain protein AF-6 is a binding partner of the Rap1A GTPase and associates with the actin cytoskeletal regulator profilin. Proc Natl Acad Sci USA. 2000;97:9064-9069.
22. Saito S, Matsushima M, Shirahama S, Minaguchi T, Kanamori Y, Minami M, Nakamura Y. Complete genomic structure DNA polymorphisms, and alternative splicing of the human AF-6 gene. DNA Res. 1998;5:115-120.
23. Ackah E, Yu J, Zoellner S, Iwakiri Y, Skurk C, Shibata R, Ouchi N, Easton RM, Galasso G, Birnbaum MJ, Walsh K, Sessa WC. Akt1/protein kinase Balpha is critical for ischemic and VEGF-mediated angiogenesis. J Clin Invest. 2005;115:2119-2127.
24. Silvestre JS, Tamarat R, Ebrahimian TG, Le-Roux A, Clergue M, Emmanuel F, Duriez M, Schwartz B, Branellec D, Levy BI. Vascular endothelial growth factor-B promotes in vivo angiogenesis. Circ Res. 2003;93:114-123.
25. Rikitake Y, Hirata K, Kawashima S, Ozaki M, Takahashi T, Ogawa W, Inoue N, Yokoyama M. Involvement of endothelial nitric oxide in sphingosine-1- phosphate-induced angiogenesis. Arterioscler Thromb Vasc Biol. 2002;22:108-114.
26. Kanzaki N, Ogita H, Komura H, Ozaki M, Sakamoto Y, Majima T, Ijuin T, Takenawa T, Takai Y. Involvement of the nectin-afadin complex in PDGF-induced cell survival. J Cell Sci. 2008;121:2008-2017.
27. Igarashi J, Michel T. Sphingosine 1-phosphate and isoform-specific activation of phosphoinositide 3-kinase beta. Evidence for divergence and convergence of receptor-regulated endothelial nitric-oxide synthase signaling pathways. J Biol Chem. 2001;276:36281-36288.
28. Heller R, Chang Q, Ehrlich G, Hsieh SN, Schoenwaelder SM, Kuh-lencordt PJ, Preissner KT, Hirsch E, Wetzker R. Overlapping and distinct roles for PI3Kbeta and gamma isoforms in S1P-induced migration of human and mouse endothelial cells. Cardiovasc Res. 2008;80:96-105.
29. Graupera M, Guillermet-Guibert J, Foukas LC, Phng LK, Cain RJ, Salpekar A, Pearce W, Meek S, Millan J, Cutillas PR, Smith AJ, Ridley AJ, Ruhrberg C, Gerhardt H, Vanhaesebroeck B. Angiogenesis selectively requires the p110alpha isoform of PI3K to control endothelial cell migration. Nature. 2008;453:662-666.
30. Koni PA, Joshi SK, Temann UA, Olson D, Burkly L, Flavell RA. Conditional vascular cell adhesion molecule 1 deletion in mice: impaired lymphocyte migration to bone marrow. J Exp Med. 2001;193:741-754.
31. Ikeda W, Nakanishi H, Miyoshi J, Mandai K, Ishizaki H, Tanaka M, Togawa A, Takahashi K, Nishioka H, Yoshida H, Mizoguchi A, Nishikawa S, Takai Y. Afadin: a key molecule essential for structural organization of cell-cell junctions of polarized epithelia during embryo-genesis. J Cell Biol. 1999;146:1117-1132.
32. Takai Y, Nakanishi H. Nectin and afadin: novel organizers of intercellular junctions. J Cell Sci. 2003;116:17-27.
33. 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.
34. Ling Q, Jacovina AT, Deora A, Febbraio M, Simantov R, Silverstein RL, Hempstead B, Mark WH, Hajjar KA. Annexin II regulates fibrin homeostasis and neoangiogenesis in vivo. J Clin Invest. 2004;113:38-48.
35. Bayless KJ, Davis GE. The Cdc42 and Rac1 GTPases are required for capillary lumen formation in three-dimensional extracellular matrices. J Cell Sci. 2002;115:1123-1136.
36. Soga N, Namba N, McAllister S, Cornelius L, Teitelbaum SL, Dowdy SF, Kawamura J, Hruska KA. Rho family GTPases regulate VEGF-stimulated endothelial cell motility. Exp Cell Res. 2001;269:73-87.
37. Su L, Hattori M, Moriyama M, Murata N, Harazaki M, Kaibuchi K, Minato N. AF-6 controls integrin-mediated cell adhesion by regulating Rap1 activation through the specific recruitment of Rap1GTP and SPA-1. J Biol Chem. 2003;278:15232-15238.
38. Fukuyama T, Ogita H, Kawakatsu T, Fukuhara T, Yamada T, Sato T, Shimizu K, Nakamura T, Matsuda M, Takai Y. Involvement of the c-Src-Crk-C3G-Rap1 signaling in the nectin-induced activation of Cdc42 and formation of adherens junctions. J Biol Chem. 2005;280:815-825.
39. Sakurai A, Fukuhara S, Yamagishi A, Sako K, Kamioka Y, Masuda M, Nakaoka Y, Mochizuki N. MAGI-1 is required for Rap1 activation upon cell-cell contact and for enhancement of vascular endothelial cadherin-mediated cell adhesion. Mol Biol Cell. 2006;17:966-976.