Eph-B4 prevents venous adaptive remodeling in the adult arterial environment

Journal of Experimental Medicine

Volumn 208, Issue 3, 2011, Pages 561-575

  Muto, Akihito ^a   Yi, Tai ^a   Harrison, Kenneth D ^a   Dávalos, Alberto ^a   Fancher, Tiffany T ^b   Ziegler, Kenneth R ^a   Feigel, Amanda ^a   Kondo, Yuka ^a   Nishibe, Toshiya ^c   Sessa, William C ^a   Dardik, Alan ^a,d  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ST MARY S HOSPITAL   (United States)

^c TOKYO MEDICAL UNIVERSITY HACHIOJI MEDICAL CENTER   (Japan)

^d VA CONNECTICUT HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; EPHRIN; LIGAND; PROTEIN EPHRIN B4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY; ARTICLE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; VEIN GRAFT; VEIN WALL;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ARTERIES; CAVEOLIN 1; GENE EXPRESSION REGULATION; HUMANS; MICE; MICE, INBRED C57BL; PHOSPHORYLATION; RATS; RECEPTOR, EPHB4; SIGNAL TRANSDUCTION; VEINS;

EID: 79952718907     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20101854     Document Type: Article

References (47)

1. Abeles, D., S. Kwei, G. Stavrakis, Y. Zhang, E.T. Wang, and G. García-Cardeña. 2006. Gene expression changes evoked in a venous segment exposed to arterial flow. J. Vasc. Surg. 44:863-870. doi:10.1016/j.jvs.2006.05.043 (Pubitemid 44441757)
2. Abulrob, A., S. Giuseppin, M.F. Andrade, A. McDermid, M. Moreno, and D. Stanimirovic. 2004. Interactions of EGFR and caveolin-1 in human glioblastoma cells: evidence that tyrosine phosphorylation regulates EGFR association with caveolae. Oncogene. 23:6967-6979. doi:10.1038/sj.onc.1207911 (Pubitemid 39279997)
3. Ackah, E., J. Yu, S. Zoellner, Y. Iwakiri, C. Skurk, R. Shibata, N. Ouchi, R.M. Easton, G. Galasso, M.J. Birnbaum, et al. 2005. Akt1/protein kinase Balpha is critical for ischemic and VEGF-mediated angiogenesis. J. Clin. Invest. 115:2119-2127. doi:10.1172/JCI24726 (Pubitemid 41134153)
4. Adams, R.H., G.A. Wilkinson, C. Weiss, F. Diella, N.W. Gale, U. Deutsch, W. Risau, and R. Klein. 1999. Roles of ephrinB ligands and EphB receptors in cardiovascular development: demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis. Genes Dev. 13:295-306. doi:10.1101/gad.13.3.295 (Pubitemid 29095801)
5. Alexander, J.H., G. Hafley, R.A. Harrington, E.D. Peterson, T.B. Ferguson Jr., T.J. Lorenz, A. Goyal, M. Gibson, M.J. Mack, D. Gennevois, et al; PREVENT IV Investigators. 2005. Efficacy and safety of edifoligide, an E2F transcription factor decoy, for prevention of vein graft failure following coronary artery bypass graft surgery: PREVENT IV: a randomized controlled trial. JAMA. 294:2446-2454. doi:10.1001/jama.294.19.2446
6. Bucci, M., J.P. Gratton, R.D. Rudic, L. Acevedo, F. Roviezzo, G. Cirino, and W.C. Sessa. 2000. In vivo delivery of the caveolin-1 scaffolding domain inhibits nitric oxide synthesis and reduces inflammation. Nat. Med. 6:1362-1367. doi:10.1038/82176 (Pubitemid 32001020)
7. Cohen, A.W., R. Hnasko, W. Schubert, and M.P. Lisanti. 2004. Role of caveolae and caveolins in health and disease. Physiol. Rev. 84:1341-1379. doi:10.1152/physrev.00046.2003 (Pubitemid 39287953)
8. Conte, M.S., D.F. Bandyk, A.W. Clowes, G.L. Moneta, L. Seely, T.J. Lorenz, H. Namini, A.D. Hamdan, S.P. Roddy, M. Belkin, et al; PREVENT III Investigators. 2006. Results of PREVENT III: a multicenter, randomized trial of edifoligide for the prevention of vein graft failure in lower extremity bypass surgery. J. Vasc. Surg. 43:742-751. doi:10.1016/j.jvs.2005.12.058
9. Couet, J., S. Li, T. Okamoto, T. Ikezu, and M.P. Lisanti. 1997a. Identification of peptide and protein ligands for the caveolin-scaffolding domain. Implications for the interaction of caveolin with caveolae-associated proteins. J. Biol. Chem. 272:6525-6533. doi:10.1074/jbc.272.10.6525 (Pubitemid 27118133)
10. Couet, J., M. Sargiacomo, and M.P. Lisanti. 1997b. Interaction of a receptor tyrosine kinase, EGF-R, with caveolins. Caveolin binding negatively regulates tyrosine and serine/threonine kinase activities. J. Biol. Chem. 272:30429-30438. doi:10.1074/jbc.272.48.30429 (Pubitemid 27512253)
11. Dardik, A., A. Yamashita, F. Aziz, H. Asada, and B.E. Sumpio. 2005. Shear stress-stimulated endothelial cells induce smooth muscle cell chemotaxis via platelet-derived growth factor-BB and interleukin-1alpha. J. Vasc. Surg. 41:321-331. doi:10.1016/j.jvs.2004.11.016 (Pubitemid 40342485)
12. Desai, N.D., E.A. Cohen, C.D. Naylor, and S.E. Fremes; Radial Artery Patency Study Investigators. 2004. A randomized comparison of radial-artery and saphenous-vein coronary bypass grafts. N. Engl. J. Med. 351:2302-2309. doi:10.1056/NEJMoa040982
13. Erber, R., U. Eichelsbacher, V. Powajbo, T. Korn, V. Djonov, J. Lin, H.P. Hammes, R. Grobholz, A. Ullrich, and P. Vajkoczy. 2006. EphB4 controls blood vascular morphogenesis during postnatal angiogenesis. EMBO J. 25:628-641. doi:10.1038/sj.emboj.7600949 (Pubitemid 43237669)
14. Fernández-Hernando, C., M. Fukata, P.N. Bernatchez, Y. Fukata, M.I. Lin, D.S. Bredt, and W.C. Sessa. 2006. Identification of Golgi-localized acyl transferases that palmitoylate and regulate endothelial nitric oxide synthase. J. Cell Biol. 174:369-377. doi:10.1083/jcb.200601051 (Pubitemid 44156767)
15. Foo, S.S., C.J. Turner, S. Adams, A. Compagni, D. Aubyn, N. Kogata, P. Lindblom, M. Shani, D. Zicha, and R.H. Adams. 2006. Ephrin-B2 controls cell motility and adhesion during blood-vessel-wall assembly. Cell. 124:161-173. doi:10.1016/j.cell.2005.10.034 (Pubitemid 43069317)
16. Foubert, P., J.S. Silvestre, B. Souttou, V. Barateau, C. Martin, T.G. Ebrahimian, C. Leré-Déan, J.O. Contreres, E. Sulpice, B.I. Levy, et al. 2007. PSGL-1-mediated activation of EphB4 increases the proangiogenic potential of endothelial progenitor cells. J. Clin. Invest. 117:1527-1537. doi:10.1172/JCI28338 (Pubitemid 46871337)
17. Fulton, D., J.P. Gratton, T.J. McCabe, J. Fontana, Y. Fujio, K. Walsh, T.F. Franke, A. Papapetropoulos, and W.C. Sessa. 1999. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature. 399: 597-601. doi:10.1038/21218
18. García-Cardeña, G., P. Martasek, B.S. Masters, P.M. Skidd, J. Couet, S. Li, M.P. Lisanti, and W.C. Sessa. 1997. Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the nos caveolin binding domain in vivo. J. Biol. Chem. 272:25437-25440. doi:10.1074/jbc.272.41.25437 (Pubitemid 27438846)
19. Gerety, S.S., H.U. Wang, Z.F. Chen, and D.J. Anderson. 1999. Symmetrical mutant phenotypes of the receptor EphB4 and its specific transmembrane ligand ephrin-B2 in cardiovascular development. Mol. Cell. 4:403-414. doi:10.1016/S1097-2765(00)80342-1 (Pubitemid 29499793)
20. Gratton, J.P., J. Fontana, D.S. O'Connor, G. Garcia-Cardena, T.J. McCabe, and W.C. Sessa. 2000. Reconstitution of an endothelial nitric-oxide synthase (eNOS), hsp90, and caveolin-1 complex in vitro. Evidence that hsp90 facilitates calmodulin stimulated displacement of eNOS from caveolin-1. J. Biol. Chem. 275:22268-22272. doi:10.1074/jbc.M001644200
21. Gratton, J.P., P. Bernatchez, and W.C. Sessa. 2004. Caveolae and caveolins in the cardiovascular system. Circ. Res. 94:1408-1417. doi:10.1161/01.RES.0000129178.56294.17 (Pubitemid 38780313)
22. Khot, U.N., D.T. Friedman, G. Pettersson, N.G. Smedira, J. Li, and S.G. Ellis. 2004. Radial artery bypass grafts have an increased occurrence of angiographically severe stenosis and occlusion compared with left internal mammary arteries and saphenous vein grafts. Circulation. 109:2086-2091. doi:10.1161/01.CIR.0000127570.20508.5C (Pubitemid 38620216)
23. Kibbe, M.R., E. Tzeng, S.L. Gleixner, S.C. Watkins, I. Kovesdi, A. Lizonova, M.S. Makaroun, T.R. Billiar, and R.Y. Rhee. 2001. Adenovirus-mediated gene transfer of human inducible nitric oxide synthase in porcine vein grafts inhibits intimal hyperplasia. J. Vasc. Surg. 34:156-165. doi:10.1067/mva.2001. 113983 (Pubitemid 33660705)
24. Kudo, F.A., A. Muto, S.P. Maloney, J.M. Pimiento, S. Bergaya, T.N. Fitzgerald, T.S. Westvik, J.C. Frattini, C.K. Breuer, C.H. Cha, et al. 2007. Venous identity is lost but arterial identity is not gained during vein graft adaptation. Arterioscler. Thromb. Vasc. Biol. 27:1562-1571. doi:10.1161/ATVBAHA. 107.143032 (Pubitemid 46986111)
25. Lajoie, P., E.A. Partridge, G. Guay, J.G. Goetz, J. Pawling, A. Lagana, B. Joshi, J.W. Dennis, and I.R. Nabi. 2007. Plasma membrane domain organization regulates EGFR signaling in tumor cells. J. Cell Biol. 179:341-356. doi:10.1083/jcb.200611106 (Pubitemid 350004897)
26. Loftus, I.M., M.J. McCarthy, A. Lloyd, A.R. Naylor, P.R. Bell, and M.M. Thompson. 1999. Prevalence of true vein graft aneurysms: implications for aneurysm pathogenesis. J. Vasc. Surg. 29:403-408. doi:10.1016/S0741-5214(99) 70267-3 (Pubitemid 29152261)
27. Mann, M.J., A.D. Whittemore, M.C. Donaldson, M. Belkin, M.S. Conte, J.F. Polak, E.J. Orav, A. Ehsan, G. Dell'Acqua, and V.J. Dzau. 1999. Exvivo gene therapy of human vascular bypass grafts with E2F decoy: the PREVENT single-centre, randomised, controlled trial. Lancet. 354:1493-1498. doi:10.1016/S0140-6736(99)09405-2 (Pubitemid 29502101)
28. Mayr, U., Y. Zou, Z. Zhang, H. Dietrich, Y. Hu, and Q. Xu. 2006. Accelerated arteriosclerosis of vein grafts in inducible NO synthase(-/-) mice is related to decreased endothelial progenitor cell repair. Circ. Res. 98:412-420. doi:10.1161/01.RES.0000201957.09227.6d
29. Murata, T., M.I. Lin, Y. Huang, J. Yu, P.M. Bauer, F.J. Giordano, and W.C. Sessa. 2007. Reexpression of caveolin-1 in endothelium rescues the vascular, cardiac, and pulmonary defects in global caveolin-1 knockout mice. J. Exp. Med. 204:2373-2382. doi:10.1084/jem.20062340 (Pubitemid 47529323)
30. Nicklin, S.A. 1999. Simple methods for preparing recombinant adenovirus for high-efficiency transduction of vascular cells. In Vascular Disease: Molecular Biology and Gene Therapy Protocols. A.H. Baker, editor. Humana, Totowa, NJ. 271-283.
31. Noren, N.K., G. Foos, C.A. Hauser, and E.B. Pasquale. 2006. The EphB4 receptor suppresses breast cancer cell tumorigenicity through an Abl-Crk pathway. Nat. Cell Biol. 8:815-825. doi:10.1038/ncb1438 (Pubitemid 44151584)
32. Nystrom, F.H., H. Chen, L.N. Cong, Y. Li, and M.J. Quon. 1999. Caveolin-1 interacts with the insulin receptor and can differentially modulate insulin signaling in transfected Cos-7 cells and rat adipose cells. Mol. Endocrinol. 13:2013-2024. doi:10.1210/me.13.12.2013 (Pubitemid 30637263)
33. Owens, C.D., N. Wake, J.G. Jacot, M. Gerhard-Herman, P. Gaccione, M. Belkin, M.A. Creager, and M.S. Conte. 2006. Early biomechanical changes in lower extremity vein grafts-distinct temporal phases of remodeling and wall stiffness. J. Vasc. Surg. 44:740-746. doi:10.1016/j.jvs.2006.06.005 (Pubitemid 44441767)
34. Owens, C.D., F.J. Rybicki, N. Wake, A. Schanzer, D. Mitsouras, M.D. Gerhard-Herman, and M.S. Conte. 2008. Early remodeling of lower extremity vein grafts: inflammation influences biomechanical adaptation. J. Vasc. Surg. 47:1235-1242. doi:10.1016/j.jvs.2008.01.009
35. Rizzo, V., D.P. McIntosh, P. Oh, and J.E. Schnitzer. 1998. In situ flow activates endothelial nitric oxide synthase in luminal caveolae of endothelium with rapid caveolin dissociation and calmodulin association. J. Biol. Chem. 273:34724-34729. doi:10.1074/jbc.273.52.34724 (Pubitemid 29028162)
36. Rudic, R.D., E.G. Shesely, N. Maeda, O. Smithies, S.S. Segal, and W.C. Sessa. 1998. Direct evidence for the importance of endotheliumderived nitric oxide in vascular remodeling. J. Clin. Invest. 101:731-736. doi:10.1172/JCI1699 (Pubitemid 28096068)
37. Shin, D., G. Garcia-Cardena, S. Hayashi, S. Gerety, T. Asahara, G. Stavrakis, J. Isner, J. Folkman, M.A. Gimbrone Jr., and D.J. Anderson. 2001. Expression of ephrinB2 identifies a stable genetic difference between arterial and venous vascular smooth muscle as well as endothelial cells, and marks subsets of microvessels at sites of adult neovascularization. Dev. Biol. 230:139-150. doi:10.1006/dbio.2000.9957 (Pubitemid 32171413)
38. Stabila, P.F., S.C. Wong, F.A. Kaplan, and W. Tao. 1998. Cell surface expression of a human IgG Fc chimera activates macrophages through Fc receptors. Nat. Biotechnol. 16:1357-1360. doi:10.1038/4339 (Pubitemid 28547448)
39. Steinle, J.J., C.J. Meininger, R. Forough, G. Wu, M.H. Wu, and H.J. Granger. 2002. Eph B4 receptor signaling mediates endothelial cell migration and proliferation via the phosphatidylinositol 3-kinase pathway. J. Biol. Chem. 277:43830-43835. doi:10.1074/jbc.M207221200 (Pubitemid 36157804)
40. Szilagyi, D.E., J.P. Elliott, J.H. Hageman, R.F. Smith, and C.A. Dall'olmo. 1973. Biologic fate of autogenous vein implants as arterial substitutes: clinical, angiographic and histopathologic observations in femoro-popliteal operations for atherosclerosis. Ann. Surg. 178:232-246. doi:10.1097/00000658-197309000-00002
41. Tawara, T., K. Hasegawa, Y. Sugiura, K. Harada, T. Miura, S. Hayashi, T. Tahara, M. Ishikawa, H. Yoshida, K. Kubo, et al. 2008. Complement activation plays a key role in antibody-induced infusion toxicity in monkeys and rats. J. Immunol. 180:2294-2298.
42. Veith, F.J., S.K. Gupta, E. Ascer, S. White-Flores, R.H. Samson, L.A. Scher, J.B. Towne, V.M. Bernhard, P. Bonier, W.R. Flinn, et al. 1986. Six-year prospective multicenter randomized comparison of autologous saphenous vein and expanded polytetrafluoroethylene grafts in infrainguinal arterial reconstructions. J. Vasc. Surg. 3:104-114. doi:10.1067/mva.1986.avs0030104 (Pubitemid 16186498)
43. Vihanto, M.M., C. Vindis, V. Djonov, D.P. Cerretti, and U. Huynh-Do. 2006. Caveolin-1 is required for signaling and membrane targeting of EphB1 receptor tyrosine kinase. J. Cell Sci. 119:2299-2309. doi:10.1242/jcs.02946 (Pubitemid 43960319)
44. Wang, H.U., Z.F. Chen, and D.J. Anderson. 1998. Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell. 93:741-753. doi:10.1016/S0092-8674(00) 81436-1 (Pubitemid 28257581)
45. Yamamoto, M., Y. Toya, C. Schwencke, M.P. Lisanti, M.G. Myers Jr., and Y. Ishikawa. 1998. Caveolin is an activator of insulin receptor signaling. J. Biol. Chem. 273:26962-26968. doi:10.1074/jbc.273.41.26962 (Pubitemid 28471718)
46. You, L.R., F.J. Lin, C.T. Lee, F.J. DeMayo, M.J. Tsai, and S.Y. Tsai. 2005. Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity. Nature. 435:98-104. doi:10.1038/nature03511 (Pubitemid 40655915)
47. Yu, J., S. Bergaya, T. Murata, I.F. Alp, M.P. Bauer, M.I. Lin, M. Drab, T.V. Kurzchalia, R.V. Stan, and W.C. Sessa. 2006. Direct evidence for the role of caveolin-1 and caveolae in mechanotransduction and remodeling of blood vessels. J. Clin. Invest. 116:1284-1291. doi:10.1172/JCI27100