Involvement of RhoA/Rho kinase signaling in VEGF-induced endothelial cell migration and angiogenesis in vitro

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 23, Issue 2, 2003, Pages 211-217

  Van Nieuw Amerongen, Geerten P ^a   Koolwijk, Pieter ^b   Versteilen, Amanda ^b   Van Hinsbergh, Victor W M ^a,b  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b TNO   (Netherlands)

Author keywords

Angiogenesis; Cytoskeleton; Endothelial cells; Migration; Stress fibers

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; F ACTIN; FIBRIN; GROWTH FACTOR; GUANOSINE TRIPHOSPHATASE; RECOMBINANT TUMOR NECROSIS FACTOR ALPHA; RECOMBINANT VASCULOTROPIN; RHO KINASE; RHO KINASE INHIBITOR; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN;

ADENOVIRUS; ANGIOGENESIS; ARTICLE; ATTENUATION; CELL MIGRATION; CONTROLLED STUDY; CYTOSKELETON; ENDOTHELIUM CELL; ENZYME ANALYSIS; ENZYME INHIBITION; ENZYME SPECIFICITY; GENETIC TRANSFECTION; GROWTH REGULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; THREE DIMENSIONAL IMAGING;

AMIDES; CAPILLARIES; CELL CULTURE TECHNIQUES; CELL MOVEMENT; CELLS, CULTURED; CYTOSKELETON; ENDOTHELIAL GROWTH FACTORS; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; ENZYME INHIBITORS; FIBRIN; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHOKINES; MALE; NEOVASCULARIZATION, PHYSIOLOGIC; PENIS; PYRIDINES; RHO GTP-BINDING PROTEINS; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; UMBILICAL VEINS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 0037324359     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.0000054198.68894.88     Document Type: Article

References (56)

1. Liotta LA, Steeg PS, Stetler-Stevenson WG. Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell. 1991;64: 327-336.
2. Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med. 1995;1:27-31.
3. Battegay EJ. Angiogenesis: mechanistic insights, neovascular diseases, and therapeutic prospects. J Mol Med. 1995;73:333-346.
4. Dvorak HF, Brown LF, Detmar M, Dvorak AM. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am J Pathol. 1995;146:1029-1039.
5. Nicosia RF. What is the role of vascular endothelial growth factor-related molecules in tumor angiogenesis? Am J Pathol. 1998;153:11-16.
6. Huot J, Houle F, Rousseau S, Deschesnes RG, Shah GM, Landry J. SAPK2/p38-dependent F-actin reorganization regulates early membrane blebbing during stress-induced apoptosis. J Cell Biol. 1998;143: 1361-1373.
7. Kiosses WB, Daniels RH, Otey C, Bokoch GM, Schwartz MA. A role for p21-activated kinase in endothelial cell migration. J Cell Biol. 1999;147:831-844.
8. Katoh K, Kano Y, Masuda M, Onishi H, Fujiwara K. Isolation and contraction of the stress fiber. Mol Biol Cell. 1998;9:1919-1938.
9. Ridley AJ. Stress fibres take shape. Nat Cell Biol. 1999;1:64-66.
10. Wong AJ, Pollard JD, Herman IM. Actin filament stress fibers in vascular endothelial cells in vivo. Science. 1983;219:867-869.
11. Nehls V, Drenckhahn D. Demonstration of actin filament stress fibers in microvascular endothelial cells in situ. Microvasc Res. 1991;42:103-112.
12. White GE, Gimbrone MA Jr, Fujiwara K. Factors influencing the expression of stress fibers in vascular endothelial cells in situ. J Cell Biol. 1983;97:416-424.
13. Colangelo S, Langille BL, Steiner G, Gotlieb AI. Alterations in endothelial F-actin microfilaments in rabbit aorta in hypercholesterolemia. Arterioscler Thromb Vasc Biol. 1998;18:52-56.
14. Van Nieuw Amerongen GP, van Hinsbergh VWM. Cytoskeletal effects of rho-like small guanine nucleotide-binding proteins in the vascular system. Arterioscler Thromb Vasc Biol. 2001;21:300-311.
15. Takaishi K, Sasaki T, Kato M, Yamochi W, Kuroda S, Nakamura T, Takeichi M, Takai Y. Involvement of Rho p21 small GTP-binding protein and its regulator in the HGF-induced cell motility. Oncogene. 1994;9: 273-279.
16. Aepfelbacher M, Essler M, Huber E, Sugai M, Weber PC. Bacterial toxins block endothelial wound repair: evidence that Rho GTPases control cytoskeletal rearrangements in migrating endothelial cells. Arterioscler Thromb Vasc Biol. 1997;17:1623-1629.
17. Fujisawa K, Fujita A, Ishizaki T, Saito Y, Narumiya S. Identification of the Rho-binding domain of p160ROCK, a Rho-associated coiled-coil containing protein kinase. J Biol Chem. 1996;271:23022-23028.
18. Leung T, Chen XQ, Manser E, Lim L. The p160 RhoA-binding kinase ROK-α is a member of a kinase family and is involved in the reorganization of the cytoskeleton. Mol Cell Biol. 1996;16:5313-5327.
19. Kimura K, Ito M, Amano M, Chihara K, Fukata Y, Nakafuku M, Yamamori B, Feng J, Nakano T, Okawa K, Iwamatsu A, Kaibuchi K. Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science. 1996;273:245-248.
20. Uehata M, Ishizaki T, Satoh H, Ono T, Kawahara T, Morishita T, Tamakawa H, Yamagami K, Inui J, Maekawa M, Narumiya S. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature. 1997;389:990-994.
21. Ishizaki T, Uehata M, Tamechika I, Keel J, Nonomura K, Maekawa M, Narumiya S. Pharmacological properties of Y-27632, a specific inhibitor of Rho-associated kinases. Mol Pharmacol. 2000;57:976-983.
22. Hall A. G proteins and small GTPases: distant relatives keep in touch. Science. 1998;280:2074-2075.
23. Offermanns S, Mancino V, Revel JP, Simon MI. Vascular system defects and impaired cell chemokinesis as a result of Gα13 deficiency. Science. 1997;275:533-536.
24. Lee MJ, Thangada S, Claffey KP, Ancellin N, Liu CH, Kluk M, Volpi M, Sha'afi RI, Hla T. Vascular endothelial cell adherens junction assembly and morphogenesis induced by sphingosine-l-phosphate. cell. 1999;99: 301-312.
25. Uchida S, Watanabe G, Shimada Y, Maeda M, Kawabe A, Mori A, Arii S, Uehata M, Kishimoto T, Oikawa T, Imamura M. The suppression of small GTPase rho signal transduction pathway inhibits angiogenesis in vitro and in vivo. Biochem Biophys Res Commun. 2000;269:633-640.
26. Kiosses WB, Hood J, Yang S, Gerritsen ME, Cheresh DA, Alderson N, Schwartz MA. A dominant-negative p65 PAK peptide inhibits angiogenesis. Circ Res. 2002;90:697-702.
27. Connolly JO, Simpson N, Hewlett L, Hall A. Rac regulates endothelial morphogenesis and capillary assembly. Mol Biol Cell. 2002;13: 2474-2485.
28. 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.
29. Vincent L, Soria C, Mirshahi F, Opolon P, Mishal Z, Vannier JP, Soria J, Hong L. Cerivastatin, an inhibitor of 3-hydroxy-3-methylglutaryl coenzyme A reductase, inhibits endothelial cell proliferation induced by angiogenic factors in vitro and angiogenesis in vivo models. Arterioscler Thromb Vasc Biol. 2002;22:623-629.
30. Park HJ, Kong D, Iruela-Arispe L, Begley U, Tang D, Galper JB. 3-Hydroxy-3-methylglutaryl coenzyme A reductase inhibitors interfere with angiogenesis by inhibiting the geranylgeranylation of RhoA. Circ Res. 2002;91:143-150.
31. 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.
32. Draijer R, Atsma DE, van der Laarse A, van Hinsbergh VW. cGMP and nitric oxide modulate thrombin-induced endothelial permeability: regulation via different pathways in human aortic and umbilical vein endothelial cells. Circ Res. 1995;76:199-208.
33. Koolwijk P, van Erck MG, de Vree WJ, Vermeer MA, Weich HA, Hanemaaijer R, van Hinsbergh VW. Cooperative effect of TNF-α, bFGF, and VEGF on the formation of tubular structures of human microvascular endothelial cells in a fibrin matrix: role of urokinase activity. J Cell Biol. 1996;132:1177-1188.
34. Sander EE, Ten Klooster JP, Van Delft S, Van der Kammen RA, Collard JG. Rac downregulates Rho activity; reciprocal balance between both GTPases determines cellular morphology and migratory behaviour. J Cell Biol. 1999;147:1009-1022.
35. Van Nieuw Amerongen GP, Van Delft S, Vermeer MA, Collard JG, van Hinsbergh VWM. Activation of RhoA by thrombin in endothelial hyperpermeability: role of Rho kinase and protein tyrosine kinases. Circ Res. 2000;87:335-340.
36. Van Nieuw Amerongen GP, Vermeer MA, Negre-Aminou P, Lankelma J, Emeis JJ, van Hinsbergh VWM. Simvastatin improves disturbed endothelial barrier function. Circulation. 2000;102:2803-2809.
37. Van Nieuw Amerongen GP, Draijer R, Vermeer MA, Van Hinsbergh VWM. Transient and prolonged increase in endothelial permeability induced by histamine and thrombin: role of protein kinases, calcium, and RhoA. Circ Res. 1998;83:1115-1123.
38. Lauder H, Frost EE, Hiley R, Fan T-PD. Quantification of the repair process involved in the repair of a cell monolayer using an in vitro model of mechanical injury. Angiogenesis. 1998;2:67-80.
39. Abedi H, Zachary I. Vascular endothelial growth factor stimulates tyrosine phosphorylation and recruitment to new focal adhesions of focal adhesion kinase and paxillin in endothelial cells. J Biol Chem. 1997;272: 15442-15451.
40. Cohen AW, Carbajal JM, Schaeffer RCJ. VEGF stimulates tyrosine phosphorylation of β-catenin and small-pore endothelial barrier dysfunction. Am J Physiol. 1999;277:H2038-H2049.
41. Li S, Chen PC, Azuma N, Hu Y-L, Wu SZ, Sumpio BE, Shyy JYJ, Chien S. Distinct roles for the small GTPases Cdc42 and Rho in endothelial responses to shear stress. J Clin Invest. 1999;103:1141-1150.
42. Zeng H, Zhao D, Mukhopadhyay D. KDR stimulates endothelial cell migration through heterotrimeric G proteins Gq/11-mediated activation of a small GTPase Rho A. J Biol Chem. 2002;277:46791-46798.
43. Gingras D, Lamy S, Beliveau R. Tyrosine phosphorylation of the vascular endothelial-growth-factor receptor-2 (VEGFR-2) is modulated by Rho proteins. Biochem J. 2000;348:273-280.
44. Jo M, Thomas KS, Somlyo AV, Somlyo AP, Gonias SL. Cooperativity between the Ras-ERK and Rho-Rho kinase pathways in urokinase-type plasminogen activator-stimulated cell migration. J Biol Chem. 2002;277:12479-12485.
45. Worthylake RA, Lemoine S, Watson JM, Burridge K. RhoA is required for monocyte tail retraction during transendothelial migration. J Cell Biol. 2001;154:147-160.
46. White GE, Fuhro RL, Stemerman MB. Reversible changes in stress fiber expression and cell shape in regenerating rat and rabbit aortic endothelium. Eur J Cell Biol. 1988;46:342-351.
47. Nobes CD, Hall A. Rho GTPases control polarity, protrusion, and adhesion during cell movement. J Cell Biol. 1999;144:1235-1244.
48. Laufs U, Liao JK. Post-transcriptional regulation of endothelial nitric oxide synthase mRNA stability by Rho GTPase. J Biol Chem. 1998;273: 24266-24271.
49. Kureishi Y, Luo Z, Shiojima I, Bialik A, Fulton D, Lefer DJ, Sessa WC, Walsh K. The HMG-CoA reductase inhibitor simvastatin activates the protein kinase Akt and promotes angiogenesis in normocholesterolemic animals. Nat Med. 2000;6:1004-1010.
50. Brouet A, Sonveaux P, Dessy C, Moniotte S, Balligand JL, Feron O. Hsp90 and caveolin are key targets for the proangiogenic nitric oxide-mediated effects of statins. Circ Res. 2001;89:866-873.
51. Sata M. Biphasic effects of statins on angiogenesis. Circulation. 2002; 106:e47.
52. Weis M, Heeschen C, Glassford AJ, Cooke JP. Statins have biphasic effects on angiogenesis. Circulation. 2002;105:739-745.
53. Urbich C, Dembach E, Zeiher AM, Dimmeler S. Double-edged role of statins in angiogenesis signaling. Circ Res. 2002;90:737-744.
54. Werner N, Priller J, Laufs U, Endres M, Bohm M, Dirnagl U, Nickenig G. Bone marrow-derived progenitor cells modulate vascular reendothelialization and neointimal formation: effect of 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibition. Arterioscler Thromb Vasc Biol. 2002;22:1567-1572.
55. Essler M, Amano M, Kruse H-J, Kaibuchi K, Weber PC, Aepfelbacher M. Thrombin inactivates myosin light chain phosphatase via Rho and its target Rho kinase in human endothelial cells. J Biol Chem. 1998;273: 21867-21874.
56. Michel CC, Curry FE. Microvascular permeability. Physiol Rev. 1999; 79:703-761.