Tie-2-dependent activation of RhoA and Rac1 participates in endothelial cell motility triggered by angiopoietin-1

Blood

Volumn 102, Issue 7, 2003, Pages 2482-2490

  Cascone, Ilaria ^b   Audero, Enrica ^b   Giraudo, Enrico ^b   Napione, Lucia ^b   Maniero, Fabrizio ^b   Philips, Mark R ^b   Collard, John G ^b   Serini, Guido ^b   Bussolino, Federico ^a  

^a CANDIOLO CANCER INSTITUTE   (Italy)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ACTIN; ANGIOPOIETIN 1; ANGIOPOIETIN RECEPTOR; GUANOSINE TRIPHOSPHATASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; RAC1 PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SOS PROTEIN; TYROSINE KINASE RECEPTOR; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL MATURATION; CELL MIGRATION; CELL MOTILITY; CELL SHAPE; CELLULAR DISTRIBUTION; CHEMOKINESIS; CONTROLLED STUDY; CYTOSKELETON; ENDOTHELIUM CELL; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MUTANT; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

EID: 0141481986     PISSN: 00064971     EISSN: None     Source Type: Journal    
DOI: 10.1182/blood-2003-03-0670     Document Type: Article

References (60)

1. Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat Med. 2000;6:389-395.
2. Bussolino F, Mantovani A, Persico G. Molecular mechanisms of blood vessel formation. Trends Biochem Sci. 1997;22:251-256.
3. Suri C, Jones PF, Patan S, et al. Requisite role of angiopoietin-1, a ligand for the Tie2 receptor, during embryonic angiogenesis. Cell. 1996;87:1171-1180.
4. Suri C, McClain J, Thurston G, et al. Increased vascularization in mice overexpressing angiopoietin-1. Science. 1998;282:468-471.
5. Uemura A, Ogawa M, Hirashima M, et al. Recombinant angiopoietin-1 restores higher-order architecture of growing blood vessels in mice in the absence of mural cells. J Clin Invest. 2002;110:1619-1628.
6. Witzenbichler B, Maisonpierre PC, Jones P, Yancopoulos GD, Isner JM. Chemotactic properties of angiopoietin-1 and -2, ligands for the endothelial-specific receptor tyrosine kinase Tie2. J Biol Chem. 1998;273:18514-18521.
7. Koblizek TI, Weiss C, Yancopoulos GD, Deutsch U, Risau W. Angiopoietin-1 induces sprouting angiogenesis in vitro. Curr Biol. 1998;8:529-532.
8. Fujikawa K, de Aos Scherpensel I, Jain S, Presman E, Varticovski L. Role of PI 3-kinase in angiopoietin-1-mediated migration and attachment-dependent survival of endothelial cells. Exp Cell Res. 1999;253:663-672.
9. Master Z, Jones N, Tran J, Jones J, Kerbel RS, Dumont DJ. Dok-R plays a pivotal role in angiopoietin-1-dependent cell migration through recruitment and activation of Pak. Embo J. 2001;20:5919-5928.
10. Kim I, Kim HG, Moon S, et al. Angiopoietin-1 induces endothelial cell sprouting through the activation of focal adhesion kinase and plasmin secretion. Circ Res. 2000;86:952-959.
11. Audero E, Cascone I, Zanon I, et al. Expression of angiopoietin-1 in human glioblastomas regulates tumor-induced angiogenesis in vivo and in vitro studies. Arteriscler Thromb Vasc Biol. 2001;21:536-541.
12. Jones N, Iljin K, Dumont DJ, Alitalo K. Tie receptors: new modulators of angiogenic and lymphangiogenic responses. Nat Rev Mol Cell Biol. 2001;2:257-267.
13. Ridley AJ, Paterson HF, Johnston CL, Diekmann D, Hall A. The small GTP-binding rac regulates growth factor-induced membrane ruffling. Cell. 1992;70:401-410.
14. Menager C, Vassy J, Doliger C, Legrand Y, Karniguian A. Subcellular localization of RhoA and ezrin at membrane ruffles of human endothelial cells: differential role of collagen and fibronectin. Exp Cell Res. 1999;249:221-230.
15. Nobes CD, Hall A. Rho GTPases control polarity, protusion and adhesion during cell movemet. J Cell Biol. 1999;144:1235-1244.
16. Kraynov VS, Chamberlain C, Bokoch GM, Schwartz MA, Slabaugh S, Hahn KM. Localized Rac activation dynamics visualized in living cells. Science. 2000;290:333-337.
17. Sells MA, Pfaff A, Chernoff J. Temporal and spatial distribution of activated Pakl in fibroblasts. J Cell Biol. 2000;151:1449-1458.
18. Miyazaki K, Yano T, Schmidt DJ, et al. Rho dependent agonist induced spatio-temporal change in myosin phosphorylation in smooth muscle cells. J Biol Chem. 2001;277:725-734.
19. Paik JH, Chae S, Lee M, Thangada H. Sphingosine 1-phosphate-induced endothelial cell migration requires the expression of EDG-1 and EDG-3 receptors and Rho-dependent activation of alphavbeta3-and beta1-containing integrins. J Biol Chem. 2001;276:11830-11837.
20. Soga N, Naga N, McAllister S, et al. Rho family GTPases regulate VEGF-stimulated endothelial cell motility. Exp Cell Res. 2001;269:73-87.
21. Dormond O, Foletti A, Paroz C, Ruegg C. NSAIDs inhibit αVβ3 integrin-mediated and Cdc42/Rac-dependent endothelial-cell spreading, migration and angiogenesis. Nat Med. 2001;7:1041-1047.
22. Wojciak-Stothard B, Potempa S, Eichholtz T, Ridley AJ. Rho and Rac but not Cdc42 regulate endothelial cell permeability. J Cell Sci. 2001;114:1343-1355.
23. Braga VM, Del Maschio A, Machesky L, Dejana E. Regulation of cadherin function by Rho and Rac: modulation by junction maturation and cellular context. Mol Biol Cell. 1999;10:9-22.
24. Vouret-Craviari V, Boquet P, Pouyssegur J, Van Obberghen-Schilling E. Regulation of the actin cytoskeleton by thrombin in human endothelial cells: role of Rho proteins in endothelial barrier function. Mol Biol Cell. 1998;9:2639-2653.
25. 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.
26. Sander EE, van Delft S, ten Klooster JP, et al. Matrix-dependent Tiam1/Rac signaling in epithelial cells promotes either cell-cell adhesion or cell migration and is regulated by phpsphatidylinositol 3-kinase. J. Cell Biol. 1998;143:1385-1398.
27. Bishop AL, Hall A. Rho GTPases and their effector proteins. Biochem J. 2000;348:241-255.
28. Lim L, Manser E, Leung T, Hall C. Regulation of phosphorylation pathways by p21 GTPases: the p21 Ras-related Rho subfamily and its role in phosphorylation signalling pathways. Eur J Biochem. 1996;242:171-185.
29. Feig LA. Tools of the trade: use of dominant-inhibitory mutants of Ras-family GTPases. Nature Cell Biol. 1999;1:E25-E27.
30. Cutrupi S, Baldanzi G, Gramaglia D, et al. Src-mediated activation of alpha-diacylglycerol kinase is required for hepatocyte growth factor-induced cell motility. EMBO J. 2000;19:4614-4622.
31. Rottner K, Hall A, Small JV. Interplay between Rac and Rho in the control of substrate contact dynamics. Curr Biol. 1999;9:640-648.
32. Scita G, Tenca P, Frittoli E, et al. Signaling from Ras to Rac and beyond: not just a matter of GEFs. EMBO J. 2000;19:2393-2398.
33. Mettouchi A, Klein S, Guo W, et al. Integrin-specific activation of Rac controls progression through the G(1) phase of the cell cycle. Mol Cell. 2001:115-127.
34. Innocenti M, Frittoli E, Ponzanelli I, et al. Phosphoinositide 3-kinase activates Rac by entering in a complex with Eps8, Abi1, and Sos-1. J Cell Biol. 2003;160:17-23.
35. Bussolino F, Di Renzo MF, Ziche M, et al. Hepatocyte growth factor is a potent angiogenic factor which stimulates endothelial cells motility and growth. J Cell Biol. 1992;119:629-641.
36. Primo L, Roca C, Ferrandi C, Lanfrancone L, Bussolino F. Human endothelial cells expressing polyoma middle T induce tumors. Oncogene. 2000;19:3632-3641.
37. Michaelson D, Silletti J, Murphy G, D'Eustachio P, Rush M, Philips MR. Differential localization of Rho GTPases in live cells: regulation by hypervariable regions and RhoGDI binding. J Cell Biol. 2001;152:111-126.
38. Serini G, Ambrosi D, Giraudo E, Gamba A, Preziosi L, Bussolino F. Modeling the early stages of vascular network assembly. EMBO J. 2003;22:1771-1779.
39. Soldi R, Mitola S, Strasly M, Defilippi P, Tarone G, Bussolino F. Role of alphavbeta3 integrin in the activation of vascular endothelial growth factor receptor-2. EMBO J. 1999;18:882-892.
40. Li Z, Aizenman CD, Cline HT. Regulation of rho GTPases by crosstalk and neuronal activity in vivo. Neuron. 2002;33:741-750.
41. Hannah MJ, Weiss U, Huttner WB. Differential extraction of proteins from paraformaldehyde-fixed cells: lessons from synaptophysin and other membrane proteins. Methods. 1998;16:170-181.
42. Jiménez C, Portela RA, Mellado M, et al. Role of the PI3K regulatory subunit in the control of actin organization and cell migration. J Cell Biol. 2000;151:249-261.
43. Kontos CD, Stauffer TP, Wen-Pin Y, et al. Tyrosine 1101 of Tie2 is the major site of association of p85 and is required for activation of phosphatidylinositol 3-kinase and Akt. Mol Cell Biol. 1998;18:4131-4140.
44. Das B, Shu X, Day GJ, et al. Control of intramolecular interactions between the pleckstrin homology and Dbl homology domains of Vav and Sos1 regulates Rac binding. J Biol Chem. 2000;275:15074-15081.
45. Chung CY, Funamoto S, Firtel RA. Signaling pathways controlling cell polarity and chemotaxis. Trends Biochem Sci. 2001;26:557-566.
46. Boivin D, Beliveau R. Subcellular distribution and membrane association of Rho-related small GTP-binding proteins in kidney cortex. Am J Physiol. 1995;269:F180-F189.
47. Kranenburg O, Poland M, Gebbink M, Oomen L, Moolenaar WH. Dissociation of LPA-induced cytoskeletal contraction from stress fibers formation by differential localization of RhoA. J Cell Sci. 1997;110:2417-2427.
48. Radhakrishna H, Al-Awar O, Khachikian Z, Donaldson JG. ARF6 requirement for rac ruffling suggests a role for membrane trafficking in cortical actin rearrangements. J Cell Sci. 1999;112:855-866.
49. Read PW, Nakamoto RK. Expression and purification of Rho/RhoGDI complexes. Meth Enzymol. 2000;325:15-25.
50. Del Pozo MA, Kiosses WB, Alderson NB, Meller N, Hahn KM, Schwartz MA. Integrins regulate GTP-Rac localized effector interactions through dissociation of Rho-GDI. Nat Cell Biol. 2002;4:232-239.
51. Michiels F, Habets GG, Stam JC, van der Kammen RA, Collard JG. A role for Rac in Tiam1-induced membrane ruffling and invasion. Nature. 1995;375:338-340.
52. Hansen MD, Nelson WJ. Serum-activated assembly and membrane translocation of an endogenous Rac1:effector complex. Curr Biol. 2001;11:356-360.
53. Kiosses WB, Daniels RH, Otey C, Bokoch CO, Schwartz MA. A role for p21-activated kinase in endothelial cell migration. J Cell Biol. 1999;147:831-843.
54. Leeuwen FN, Kain HE, Kammen RA, Michiels F, Kranenburg OW, Collard JG. The guanine nucleotide exchange factor Tiam1 affects neuronal morphology; opposing roles for the small GTPases Rac and Rho. J Cell Biol. 1997;139:797-807.
55. Fanto M, Weber U, Strutt DI, Mlodzik M. Nuclear signaling by Rac and Rho GTPases is required in the establishment of epithelial planar polarity in the Drosophila eye. Curr Biol. 2000;10:979-988.
56. Sander E, ten Klooster JP, van Defft S, van der Kammen RA, Collard J. Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behaviour. J Cell Biol. 1999;147:1009-1021.
57. Marinissen MJ, Chiariello M, Gutkind JS. Regulation of gene expression by the small GTPase Rho through the ERK6 (p38 gamma) MAP kinase pathway. Genes Dev. 2001;15:535-553.
58. Huang S, Chen LY, Zuraw BL, Ye RD, Pan ZK. Chemoattractant-stimulated NF-kappaB activation is dependent on the low molecular weight GTPase RhoA. J Biol Chem. 2001;276:40977-40981.
59. Schmidt A, Hall A. Guanine nucleotide exchange factors for Rho GTPases: tuming on the switch. Genes Dev. 2002;16:1587-1609.
60. Han J, Luby-Phelps K, Das B, et al. Role of substrates and products of PI 3-kinase in regulating activation of Rac-related guanosine triphosphatases by Vav. Science. 1998;279:558-560.