Vascular endothelial growth factor-stimulated actin reorganization and migration of endothelial cells is regulated via the serine/threonine kinase Akt

Circulation Research

Volumn 86, Issue 8, 2000, Pages 892-896

  Morales Ruiz, Manuel ^a,b   Fulton, David ^a,b   Sowa, Grzegorz ^a,b   Languino, Lucia R ^a   Fujio, Yasushi ^c   Walsh, Kenneth ^c   Sessa, William C ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ST ELIZABETH'S MEDICAL CENTER   (United States)

Author keywords

Actin; Angiogenesis; Cell migration; Nitric oxide; Vascular endothelial growth factor

Indexed keywords

ACTIN; BETA GALACTOSIDASE; NITRIC OXIDE SYNTHASE; PROTEIN SERINE THREONINE KINASE; VASCULOTROPIN;

ADENOVIRUS; ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; CYTOKINESIS; ENDOTHELIUM CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

EID: 0034724736     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.86.8.892     Document Type: Article

References (35)

1. Wymann MP, Pirola L. Structure and function of phosphoinositide 3-kinases. Biochim Biophys Acta. 1998;1436:127-150.
2. Leevers SJ, Weinkove D, MacDougall LK, Hafen E, Waterfield MD. The Drosophila phosphoinositide 3-kinase Dpi 10 promotes cell growth. EMBO J. 1996;15:6584-6594.
3. Schu PV, Takegawa K, Fry MJ, Stack JH, Waterfield MD, Emr SD. Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science. 1993;260:88-91.
4. Kotani K, Yonezawa K, Hara K, Ueda H, Kitamura Y, Sakaue H, Ando A, Chavanieu A, Calas B, Grigorescu F, Nishiyama M, Waterfield MD, Kasuga M. Involvement of phosphoinositide 3-kinase in insulin- or IGF-1-induced membrane ruffling. EMBO J. 1994;13:2313-2321.
5. Wennstrom S, Hawkins P, Cooke F, Hara K, Yonezawa K, Kasuga M, Jackson T, Claesson-Welsh L, Stephens L. Activation of phosphoinositide 3-kinase is required for PDGF-stimulated membrane ruffling. Curr Biol. 1994;4:385-393.
6. Rodriguez-Viciana P, Warne PH, Khwaja A, Marte BM, Pappin D, Das P, Waterfield MD, Ridley A, Downward J. Role of phosphoinositide 3-OH kinase in cell transformation and control of the actin cytoskeleton by Ras. Cell. 1997;89:457-467.
7. Franke TF, Kaplan DR, Cantley LC. PI3K: downstream AKTion blocks apoptosis. Cell. 1997;88:435-437.
8. Downward J. Mechanisms and consequences of activation of protein kinase B/Akt. Curr Opin Cell Biol. 1998;10:262-267.
9. Coffer PJ, Jin J, Woodgett JR. Protein kinase B (c-Akt): a multifunctional mediator of phosphatidylinositol 3-kinase activation. Biochem J. 1998; 335:1-13.
10. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, Franke TF, Papapetropoulos A, Sessa WC. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature. 1999;399:597-601.
11. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature. 1999;399:601-605.
12. Michell BJ, Griffiths JE, Mitchelhill KJ, Rodriguez-Crespo I, Tiganis T, Bozinovski S, de Montellano PO, Kemp BE, Pearson RB. The Akt kinase signals directly to endothelial nitric oxide synthase. Curr Biol. 1999;9: 845-848.
13. Noiri E, Hu Y, Bahou WF, Keese CR, Giaever I, Goligorsky MS. Permissive role of nitric oxide in endothelin-induced migration of endothelial cells. J Biol Chem. 1997;272:1747-1752.
14. Ziche M, Morbidelli L, Masini E, Amerini S, Granger HJ, Maggi CA, Geppetti P, Ledda F. Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. J Clin Invest. 1994;94:2036-2044.
15. Goligorsky MS, Abedi H, Noiri E, Takhtajan A, Lense S, Romanov V, Zachary I. Nitric oxide modulation of focal adhesions in endothelial cells. Am J Physiol. 1999;276:C1271-C1281.
16. Garcia-Cardena G, Fan R, Stern DF, Liu J, Sessa WC. Endothelial nitric oxide synthase is regulated by tyrosine phosphorylation and interacts with caveolin-1. J Biol Chem. 1996;271:27237-27240.
17. Del Vecchio PJ, Siflinger-Birnboim A, Belloni PN, Holleran LA, Lum H, Malik AB. Culture and characterization of pulmonary microvascular endothelial cells. In Vitro Cell Dev Biol. 1992;28A:711-715.
18. Sessa WC, García-Cardeña G, Liu J, Keh A, Pollock JS, Bradley J, Thiru S, Braverman IM, Desai KM. The Golgi association of endothelial nitric oxide synthase is necessary for the efficient synthesis of nitric oxide. J Biol Chem. 1995;270:17641-17644.
19. Fujio Y, Walsh K. Akt mediates cytoprotection of endothelial cells by vascular endothelial growth factor in an anchorage-dependent manner. J Biol Chem. 1999;274:16349-16354.
20. Shimonaka M, Yamaguchi Y. Purification and biological characterization of epitaxin, a fibroblast-derived motility factor for epithelial cells. J Biol Chem. 1994;269:14284-14289.
21. Sowa G, Liu J, Papapetropoulos A, Rex-Haffner M, Hughes TE, Sessa WC. Trafficking of endothelial nitric-oxide synthase in living cells: quantitative evidence supporting the role of palmitoylation as a kinetic trapping mechanism limiting membrane diffusion. J Biol Chem. 1999;274: 22524-22531.
22. Waltenberger J, Claesson-Welsh L, Siegbahn A, Shibuya M, Heldin CH. Different signal transduction properties of KDR and Flt1, two receptors for vascular endothelial growth factor. J Biol Chem. 1994;269:26988-26995.
23. Languino LR, Gehlsen KR, Wayner E, Carter WG, Engvall E, Ruoslahti E. Endothelial cells use alpha 2 beta 1 integrin as a laminin receptor. J Cell Biol. 1989;109:2455-2462.
24. Papapetropoulos A, Garcia-Cardena G, Madri JA, Sessa WC. Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J Clin Invest. 1997;100:3131-3139.
25. Murohara T, Asahara T, Silver M, Bauters C, Masuda H, Kalka C, Keamey M, Chen D, Symes JF, Fishman MC, Huang PL, Isner JM. Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest. 1998;101:2567-2578.
26. Rousseau S, Houle F, Landry J, Huot J. p38 MAP kinase activation by vascular endothelial growth factor mediates actin reorganization and cell migration in human endothelial cells. Oncogene. 1997;15:2169-2177.
27. Meili R, Ellsworth C, Lee S, Reddy TB, Ma H, Firtel RA. Chemoattractant-mediated transient activation and membrane localization of Akt/PKB is required for efficient chemotaxis to cAMP in Dictyostelium. EMBO J. 1999; 18:2092-2105.
28. Ziehe M, Morbidelli L, Choudhuri R, Zhang HT, Donnini S, Granger HJ, Bicknell R. Nitric oxide synthase lies downstream from vascular endothelial growth factor-induced but not basic fibroblast growth factor-induced angiogenesis. J Clin Invest. 1997;99:2625-2634.
29. Parenti A, Morbidelli L, Cui XL, Douglas JG, Hood JD, Granger HJ, Ledda F, Ziehe M. Nitric oxide is an upstream signal of vascular endothelial growth factor-induced extracellular signal-regulated kinase 1/2 activation in postcapillary endothelium. J Biol Chem. 1998;273:4220-4226.
30. Bellacosa A, Testa JR, Staal SP, Tsichlis PN. A retroviral oncogene, akt, encoding a serine-threonine kinase containing an SH2-like region. Science. 1991;254:274-277.
31. Ahmed NN, Franke TF, Bellacosa A, Datta K, Gonzalez-Portal ME, Taguchi T, Testa JR, Tsichlis PN. The proteins encoded by c-akt and v-akt differ in post-translational modification, subcellular localization and oncogenic potential. Oncogene. 1993;8:1957-1963.
32. Andjelkovic M, Alessi DR, Meier R, Fernandez A, Lamb NJ, Frech M, Cron P, Cohen P, Lucocq JM, Hemmings BA. Role of translocation in the activation and function of protein kinase B. J Biol Chem. 1997;272: 31515-31524.
33. Astoul E, Watton S, Cantrell D. The dynamics of protein kinase B regulation during B cell antigen receptor engagement. J Cell Biol. 1999;145:1511-1520.
34. Chen ZP, Mitchelhill KI, Michell BJ, Stapleton D, Rodriguez-Crespo I, Witters LA, Power DA, Ortiz de Montellano PR, Kemp BE. AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS Lett. 1999; 443:285-289.
35. He H, Venema VJ, Gu X, Venema RC, Marrero MB, Caldwell RB. Vascular endothelial growth factor signals endothelial cell production of nitric oxide and prostacyclin through flk-1/KDR activation of c-Src. J Biol Chem. 1999; 274:25130-25135.