© 2000 American Heart Association, Inc.
Cellular Biology |
Vascular Endothelial Growth Factor–Stimulated Actin Reorganization and Migration of Endothelial Cells Is Regulated via the Serine/Threonine Kinase Akt
From the Departments of Pharmacology (M.M.-R., D.F., G.S., W.C.S.) and Pathology (L.R.L.) and Molecular Cardiobiology Program (M.M.-R., D.F., G.S., W.C.S.), Boyer Center for Molecular Medicine, Yale University School of Medicine, New Haven, Conn, and Division of Cardiovascular Research (Y.F., K.W.), St Elizabeth’s Medical Center, Boston, Mass.
Correspondence to William C. Sessa, Yale University School of Medicine, Boyer Center for Molecular Medicine, 295 Congress Ave, New Haven, CT 06536-0812. E-mail william.sessa{at}yale.edu
Abstract—Vascular endothelial growth factor (VEGF) induces endothelial cell proliferation, migration, and actin reorganization, all necessary components of an angiogenic response. However, the distinct signal transduction mechanisms leading to each angiogenic phenotype are not known. In this study, we examined the ability of VEGF to stimulate cell migration and actin rearrangement in microvascular endothelial cells infected with adenoviruses encoding ß-galactosidase (ß-gal), activation-deficient Akt (AA-Akt), or constitutively active Akt (myr-Akt). VEGF increased cell migration in cells transduced with ß-gal, whereas AA-Akt blocked VEGF-induced cell locomotion. Interestingly, myr-Akt transduction of bovine lung microvascular endothelial cells stimulated cytokinesis in the absence of VEGF, suggesting that constitutively active Akt, per se, can initiate the process of cell migration. Treatment of ß-gal–infected endothelial cells with an inhibitor of NO synthesis blocked VEGF-induced migration but did not influence migration initiated by myr-Akt. In addition, VEGF stimulated remodeling of the actin cytoskeleton into stress fibers, a response abrogated by infection with dominant-negative Akt, whereas transduction with myr-Akt alone caused profound reorganization of F-actin. Collectively, these data demonstrate that Akt is critically involved in endothelial cell signal transduction mechanisms leading to migration and that the Akt/endothelial NO synthase pathway is necessary for VEGF-stimulated cell migration.
Key Words: vascular endothelial growth factor • angiogenesis • cell migration • nitric oxide • actin
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C. Urbich, E. Dernbach, A. M. Zeiher, and S. Dimmeler Double-Edged Role of Statins in Angiogenesis Signaling Circ. Res., April 5, 2002; 90(6): 737 - 744. [Abstract] [Full Text] [PDF]
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T. Suhara, H.-S. Kim, L. A. Kirshenbaum, and K. Walsh Suppression of Akt Signaling Induces Fas Ligand Expression: Involvement of Caspase and Jun Kinase Activation in Akt-Mediated Fas Ligand Regulation Mol. Cell. Biol., January 15, 2002; 22(2): 680 - 691. [Abstract] [Full Text] [PDF]
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 J.N. UPALAKALIN, I. HEMO, C. DEHIO, E. KESHET, and L.E. BENJAMIN Survival Mechanisms of VEGF and PlGF during Microvascular Remodeling Cold Spring Harb Symp Quant Biol, January 1, 2002; 67(0): 181 - 188. [Abstract] [PDF]
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C. Urbich, E. Dernbach, A. Reissner, M. Vasa, A. M. Zeiher, and S. Dimmeler Shear Stress-Induced Endothelial Cell Migration Involves Integrin Signaling Via the Fibronectin Receptor Subunits {alpha}5 and {beta}1 Arterioscler Thromb Vasc Biol, January 1, 2002; 22(1): 69 - 75. [Abstract] [Full Text] [PDF]
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 P. M. Becker, A. D. Verin, M. A. Booth, F. Liu, A. Birukova, and J. G. N. Garcia Differential regulation of diverse physiological responses to VEGF in pulmonary endothelial cells Am J Physiol Lung Cell Mol Physiol, December 1, 2001; 281(6): L1500 - L1511. [Abstract] [Full Text] [PDF]
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A. P. McLaughlin and G. W. De Vries Role of PLCgamma and Ca2+ in VEGF- and FGF-induced choroidal endothelial cell proliferation Am J Physiol Cell Physiol, November 1, 2001; 281(5): C1448 - C1456. [Abstract] [Full Text] [PDF]
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 D. A. Flusberg, Y. Numaguchi, and D. E. Ingber Cooperative Control of Akt Phosphorylation, bcl-2 Expression, and Apoptosis by Cytoskeletal Microfilaments and Microtubules in Capillary Endothelial Cells Mol. Biol. Cell, October 1, 2001; 12(10): 3087 - 3094. [Abstract] [Full Text] [PDF]
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 T. Hayashibara, Y. Yamada, T. Miyanishi, H. Mori, T. Joh, T. Maeda, N. Mori, T. Maita, S. Kamihira, and M. Tomonaga Vascular Endothelial Growth Factor and Cellular Chemotaxis: A Possible Autocrine Pathway in Adult T-Cell Leukemia Cell Invasion Clin. Cancer Res., September 1, 2001; 7(9): 2719 - 2726. [Abstract] [Full Text] [PDF]
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 F. Liu, A. D. Verin, P. Wang, R. Day, R. P. Wersto, F. J. Chrest, D. K. English, and J. G. N. Garcia Differential Regulation of Sphingosine-1-Phosphate- and VEGF-Induced Endothelial Cell Chemotaxis . Involvement of Gialpha 2-Linked Rho Kinase Activity Am. J. Respir. Cell Mol. Biol., June 1, 2001; 24(6): 711 - 719. [Abstract] [Full Text] [PDF]
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M. Mesri, M. Morales-Ruiz, E. J. Ackermann, C. F. Bennett, J. S. Pober, W. C. Sessa, and D. C. Altieri Suppression of Vascular Endothelial Growth Factor-Mediated Endothelial Cell Protection by Survivin Targeting Am. J. Pathol., May 1, 2001; 158(5): 1757 - 1765. [Abstract] [Full Text] [PDF]
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E. Chavakis, E. Dernbach, C. Hermann, U. F. Mondorf, A. M. Zeiher, and S. Dimmeler Oxidized LDL Inhibits Vascular Endothelial Growth Factor-Induced Endothelial Cell Migration by an Inhibitory Effect on the Akt/Endothelial Nitric Oxide Synthase Pathway Circulation, April 24, 2001; 103(16): 2102 - 2107. [Abstract] [Full Text] [PDF]
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H. Nakagami, R. Morishita, K. Yamamoto, Y. Taniyama, M. Aoki, K. Matsumoto, T. Nakamura, Y. Kaneda, M. Horiuchi, and T. Ogihara Mitogenic and Antiapoptotic Actions of Hepatocyte Growth Factor Through ERK, STAT3, and Akt in Endothelial Cells Hypertension, February 1, 2001; 37(2): 581 - 586. [Abstract] [Full Text] [PDF]
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S. Dimmeler and A. M. Zeiher Endothelial Cell Apoptosis in Angiogenesis and Vessel Regression Circ. Res., September 15, 2000; 87(6): 434 - 439. [Abstract] [Full Text] [PDF]
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D.-Q. Zheng, A. S. Woodard, G. Tallini, and L. R. Languino Substrate Specificity of alpha vbeta 3 Integrin-mediated Cell Migration and Phosphatidylinositol 3-Kinase/AKT Pathway Activation J. Biol. Chem., August 4, 2000; 275(32): 24565 - 24574. [Abstract] [Full Text] [PDF]
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M. A. Reddy, N. V. Prasadarao, C. A. Wass, and K. S. Kim Phosphatidylinositol 3-Kinase Activation and Interaction with Focal Adhesion Kinase in Escherichia coli K1 Invasion of Human Brain Microvascular Endothelial Cells J. Biol. Chem., November 17, 2000; 275(47): 36769 - 36774. [Abstract] [Full Text] [PDF]
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J.-P. Gratton, M. Morales-Ruiz, Y. Kureishi, D. Fulton, K. Walsh, and W. C. Sessa Akt Down-regulation of p38 Signaling Provides a Novel Mechanism of Vascular Endothelial Growth Factor-mediated Cytoprotection in Endothelial Cells J. Biol. Chem., August 3, 2001; 276(32): 30359 - 30365. [Abstract] [Full Text] [PDF]
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I. Kim, S.-O. Moon, S. Hoon Kim, H. Jin Kim, Y. Soon Koh, and G. Young Koh Vascular Endothelial Growth Factor Expression of Intercellular Adhesion Molecule 1 (ICAM-1), Vascular Cell Adhesion Molecule 1 (VCAM-1), and E-selectin through Nuclear Factor-kappa B Activation in Endothelial Cells J. Biol. Chem., March 2, 2001; 276(10): 7614 - 7620. [Abstract] [Full Text] [PDF]
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M. Morales-Ruiz, M.-J. Lee, S. Zollner, J.-P. Gratton, R. Scotland, I. Shiojima, K. Walsh, T. Hla, and W. C. Sessa Sphingosine 1-Phosphate Activates Akt, Nitric Oxide Production, and Chemotaxis through a Gi Protein/Phosphoinositide 3-Kinase Pathway in Endothelial Cells J. Biol. Chem., May 25, 2001; 276(22): 19672 - 19677. [Abstract] [Full Text] [PDF]
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N. J. MacDonald, W. Y. Shivers, D. L. Narum, S. M. Plum, J. N. Wingard, S. R. Fuhrmann, H. Liang, J. Holland-Linn, D. H. T. Chen, and B. K. L. Sim Endostatin Binds Tropomyosin. A POTENTIAL MODULATOR OF THE ANTITUMOR ACTIVITY OF ENDOSTATIN J. Biol. Chem., June 29, 2001; 276(27): 25190 - 25196. [Abstract] [Full Text] [PDF]
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K. N. Meadows, P. Bryant, and K. Pumiglia Vascular Endothelial Growth Factor Induction of the Angiogenic Phenotype Requires Ras Activation J. Biol. Chem., December 21, 2001; 276(52): 49289 - 49298. [Abstract] [Full Text] [PDF]
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D. Thuringer, L. Maulon, and C. Frelin Rapid Transactivation of the Vascular Endothelial Growth Factor Receptor KDR/Flk-1 by the Bradykinin B2 Receptor Contributes to Endothelial Nitric-oxide Synthase Activation in Cardiac Capillary Endothelial Cells J. Biol. Chem., January 11, 2002; 277(3): 2028 - 2032. [Abstract] [Full Text] [PDF]
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T. Suhara, T. Mano, B. E. Oliveira, and K. Walsh Phosphatidylinositol 3-Kinase/Akt Signaling Controls Endothelial Cell Sensitivity to Fas-Mediated Apoptosis via Regulation of FLICE-Inhibitory Protein (FLIP) Circ. Res., July 6, 2001; 89(1): 13 - 19. [Abstract] [Full Text] [PDF]
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M. Vasa, S. Fichtlscherer, K. Adler, A. Aicher, H. Martin, A. M. Zeiher, and S. Dimmeler Increase in Circulating Endothelial Progenitor Cells by Statin Therapy in Patients With Stable Coronary Artery Disease Circulation, June 19, 2001; 103(24): 2885 - 2890. [Abstract] [Full Text] [PDF]
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C. Urbich, E. Dernbach, A. M. Zeiher, and S. Dimmeler Double-Edged Role of Statins in Angiogenesis Signaling Circ. Res., April 5, 2002; 90(6): 737 - 744. [Abstract] [Full Text] [PDF]
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