Role of the small GTPase Rap1 for integrin activity regulation in endothelial cells and angiogenesis

Blood

Volumn 113, Issue 2, 2009, Pages 488-497

  Carmona, Guillaume ^a   Göttig, Stephan ^a   Orlandi, Alessia ^a   Scheele, Jürgen ^b   Bäuerle, Tobias ^c   Jugold, Manfred ^c   Kiessling, Fabian ^c,d   Henschler, Reinhard ^a   Zeiher, Andreas M ^a   Dimmeler, Stefanie ^a   Chavakis, Emmanouil ^a  

^a GOETHE UNIVERSITY   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; BETA1 INTEGRIN; FOCAL ADHESION KINASE; GUANOSINE TRIPHOSPHATASE; PROTEIN KINASE B; RAP1 PROTEIN; RAP1A PROTEIN; RAP1B PROTEIN; TYROSINE DERIVATIVE; UNCLASSIFIED DRUG; VASCULOTROPIN; AKT1 PROTEIN, HUMAN; FIBROBLAST GROWTH FACTOR; FOCAL ADHESION KINASE 1; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN; PTK2 PROTEIN, HUMAN; RAP PROTEIN; RAP1A PROTEIN, HUMAN; RAP1B PROTEIN, HUMAN; RAP1B PROTEIN, MOUSE; RAP1GAP PROTEIN, HUMAN; RAPL PROTEIN, MOUSE; RASSF5 PROTEIN, HUMAN;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; GENE ACTIVITY; GENE CONTROL; GENE OVEREXPRESSION; GENE SILENCING; HETEROZYGOTE; HUMAN; HUMAN CELL; LIMB ISCHEMIA; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PHOSPHORYLATION; SPROUTING; UMBILICAL VEIN; WILD TYPE; ANIMAL; CELL MOTION; CYTOLOGY; ENZYMOLOGY; HINDLIMB; ISCHEMIA; METABOLISM; MOUSE MUTANT; PHOSPHORYLATION; PHYSIOLOGY; VASCULARIZATION;

ANIMALS; ANTIGENS, CD29; CELL ADHESION; CELL MOVEMENT; ENDOTHELIAL CELLS; FIBROBLAST GROWTH FACTORS; FOCAL ADHESION KINASE 1; GENE SILENCING; GTPASE-ACTIVATING PROTEINS; HINDLIMB; HUMANS; ISCHEMIA; MICE; MICE, KNOCKOUT; MONOMERIC GTP-BINDING PROTEINS; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RAP GTP-BINDING PROTEINS; RAP1 GTP-BINDING PROTEINS; UMBILICAL VEINS;

EID: 58849159701     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-02-138438     Document Type: Article

References (63)

1. Carmeliet P. Mechanisms of angiogenesis and arteriogenesis. Nat Med. 2000;6:389-395.
2. Chavakis E, Dimmeler S. Regulation of endothelial cell survival and apoptosis during angiogenesis. Arterioscler Thromb Vasc Biol. 2002;22:887-893.
3. Ferrara N. The role of VEGF in the regulation of physiological and pathological angiogenesis. EXS. 2005:209-231.
4. Presta M, Dell'Era P, Mitola S, Moroni E, Ronca R, Rusnati M. Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis. Cytokine Growth Factor Rev. 2005;16:159-178.
5. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell. 2002;110:673-687.
6. Hynes RO. Cell-matrix adhesion in vascular development. J Thromb Haemost. 2007;5[Suppl 1]:32-40.
7. Byzova TV, Goldman CK, Pampori N, et al. A mechanism for modulation of cellular responses to VEGF: activation of the integrins. Mol Cell. 2000;6:851-860.
8. Ohmstede CA, Farrell FX, Reep BR, Clemetson KJ, Lapetina EG. RAP2B: a RAS-related GTP-binding protein from platelets. Proc Natl Acad Sci U S A. 1990;87:6527-6531.
9. Bos JL. Ras-like GTPases. Biochim Biophys Acta. 1997;1333:M19-M31.
10. Bos JL, de Rooij J, Reedquist KA. Rap1 signalling: adhering to new models. Nat Rev Mol Cell Biol. 2001;2:369-377.
11. Bos JL. Linking Rap to cell adhesion. Curr Opin Cell Biol. 2005;17:123-128.
12. Paganini S, Guidetti GF, Catricala S, et al. Identification and biochemical characterization of Rap2C, a new member of the Rap family of small GTP-binding proteins. Biochimie. 2006;88:285-295.
13. Bos JL, Rehmann H, Wittinghofer A. GEFs and GAPs: critical elements in the control of small G proteins. Cell. 2007;129:865-877.
14. Reedquist KA, Ross E, Koop EA, et al. The small GTPase, Rap1, mediates CD31-induced integrin adhesion. J Cell Biol. 2000;148:1151-1158.
15. Caron E, Self AJ, HallA. The GTPase Rap1 controls functional activation of macrophage integrin alphaMbeta2 by LPS and other inflammatory mediators. Curr Biol. 2000;10:974-978.
16. AraiA, Nosaka Y, Kanda E, Yamamoto K, Miyasaka N, Miura O. Rap1 is activated by erythropoietin or interleukin-3 and is involved in regulation of beta1 integrin-mediated hematopoietic cell adhesion. J Biol Chem. 2001;276:10453-10462.
17. Prevost N, Woulfe D, Tanaka T, Brass LF. Interactions between Eph kinases and ephrins provide a mechanism to support platelet aggregation once cell-to-cell contact has occurred. Proc Natl Acad Sci U S A. 2002;99:9219-9224.
18. Woulfe D, Jiang H, Mortensen R, Yang J, Brass LF. Activation of Rap1B by G(i) family members in platelets. J Biol Chem. 2002;277:23382-23390.
19. Bertoni A, Tadokoro S, Eto K, et al. Relationships between Rap1b, affinity modulation of integrin alpha IIbbeta 3, and the actin cytoskeleton. J Biol Chem. 2002;277:25715-25721.
20. Rangarajan S, Enserink JM, Kuiperij HB, et al. Cyclic AMP induces integrin-mediated cell adhesion through Epac and Rap1 upon stimulation of the beta 2-adrenergic receptor. J Cell Biol. 2003; 160:487-493.
21. Shimonaka M, Katagiri K, Nakayama T, et al. Rap1 translates chemokine signals to integrin activation, cell polarization, and motility across vascular endothelium under flow. J Cell Biol. 2003;161:417-427.
22. Chrzanowska-Wodnicka M, Smyth SS, Schoenwaelder SM, Fischer TH, White GC 2nd. Rap1b is required for normal platelet function and hemostasis in mice. J Clin Invest. 2005;115:680-687.
23. Lorenowicz MJ, van Gils J, de Boer M, Hordijk PL, Fernandez-Borja M. Epac1-Rap1 signaling regulates monocyte adhesion and chemotaxis. J Leukoc Biol. 2006;80:1542-1552.
24. Carmona G, Chavakis E, Koehl U, Zeiher AM, Dimmeler S. Activation of Epac stimulates integrin-dependent homing of progenitor cells. Blood. 2008;111:2640-2646.
25. Chrzanowska-Wodnicka M, Kraus AE, Gale D, White GC 2nd, Vansluys J. Defective angiogen-esis, endothelial migration, proliferation, and MAPK signaling in Rap1b-deficient mice. Blood. 2008;111:2647-2656.
26. Fujita H, Fukuhara S, Sakurai A, et al. Local activation of Rap1 contributes to directional vascular endothelial cell migration accompanied by extension of microtubules on which RAPL, a Rap1-as-sociating molecule, localizes. J Biol Chem. 2005; 280:5022-5031.
27. Katagiri K, Maeda A, Shimonaka M, Kinashi T. RAPL, a Rap1-binding molecule that mediates Rap1-induced adhesion through spatial regulation of LFA-1. Nat Immunol. 2003;4:741-748.
28. Lafuente EM, van Puijenbroek AA, Krause M, et al. RIAM, an Ena/VASP and Profilin ligand, interacts with Rap1-GTP and mediates Rap1-induced adhesion. Dev Cell. 2004;7:585-595.
29. Cullere X, Shaw SK, Andersson L, Hirahashi J, Luscinskas FW, Mayadas TN. Regulation of vascular endothelial barrier function by Epac, a cAMP-activated exchange factor for Rap GT-Pase. Blood. 2005;105:1950-1955.
30. Fukuhara S, SakuraiA, Sano H, et al. Cyclic AMP potentiates vascular endothelial cadherin-medi-ated cell-cell contact to enhance endothelial barrier function through an Epac-Rap1 signaling pathway. Mol Cell Biol. 2005;25:136-146.
31. Kooistra MR, Corada M, Dejana E, Bos JL. Epac1 regulates integrity of endothelial cell junctions through VE-cadherin. FEBS Lett. 2005;579: 4966-4972.
32. Wittchen ES, Worthylake RA, Kelly P, Casey PJ, Quilliam LA, Burridge K. Rap1 GTPase inhibits leukocyte transmigration by promoting endothelial barrier function. J Biol Chem. 2005;280: 11675-11682.
33. OrlovaVV, Economopoulou M, Lupu F, Santoso S, ChavakisT. Junctional adhesion molecule-C regulates vascular endothelial permeability by modulating VE-cadherin-mediated cell-cell contacts. J Exp Med. 2006;203:2703-2714.
34. Dimmeler S, Fisslthaler B, Fleming I, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells via Akt-dependent phosphorylation. Nature. 1999;399:601-605.
35. Chavakis E, Dernbach E, Hermann C, Mondorf UF, Zeiher AM, Dimmeler S. Oxidized LDL inhibits VEGF-induced endothelial cell migration by an inhibitory effect on the Akt/eNOS pathway. Circulation. 2001;103:2102-2107.
36. BivonaTG, Wiener HH, Ahearn IM, Silletti J, Chiu VK, Philips MR. Rap1 up-regulation and activation on plasma membrane regulates T cell adhesion. J Cell Biol. 2004;164:461-470.
37. Korff T, Augustin HG. Integration of endothelial cells in multicellular spheroids prevents apoptosis and induces differentiation. J Cell Biol. 1998;143: 1341-1352.
38. Urbich C. Molecular Cardiology, Goethe University-Frankfurt, Frankfurt, Germany. Gene Expression Omnibus. www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc= GSE2040. Accessed December 5, 2004.
39. Rubinfeld B, Munemitsu S, Clark R, et al. Molecular cloning of a GTPase activating protein specific for the Krev-1 protein p21rap1. Cell. 1991;65: 1033-1042.
40. BivonaTG, Philips MR. Analysis of Ras and Rap activation in living cells using fluorescent Ras binding domains. Methods. 2005;37:138-145.
41. Ridley AJ, Schwartz MA, Burridge K, et al. Cell migration: integrating signals from front to back. Science. 2003;302:1704-1709.
42. Carman CV, Springer TA. Integrin avidity regulation: are changes in affinity and conformation underemphasized? Curr Opin Cell Biol. 2003;15: 547-556.
43. Katagiri K, Ohnishi N, Kabashima K, et al. Crucial functions of the Rap1 effector molecule RAPL in lymphocyte and dendritic cell trafficking. Nat Immunol. 2004;5:1045-1051.
44. Gotoh T, Hattori S, Nakamura S, et al. Identification of Rap1 as a target for the Crk SH3 domain-binding guanine nucleotide-releasing factor C3G. Mol Cell Biol. 1995;15:6746-6753.
45. Larsson H, Klint P, Landgren E, Claesson-Welsh L. Fibroblast growth factor receptor-1-mediated endothelial cell proliferation is dependent on the Src homology (SH) 2/SH3 domain-containing adaptor protein Crk. J Biol Chem. 1999;274: 25726-25734.
46. Stoletov KV, Gong C, Terman BI. Nck and Crk mediate distinct VEGF-induced signaling pathways that serve overlapping functions in focal adhesion turnover and integrin activation. Exp Cell Res. 2004;295:258-268.
47. Chrzanowska-Wodnicka M, Kraus AE, Gale D, White GC 2nd, Vansluys J. Defective angiogenesis, endothelial migration, proliferation and MAPK signaling in Rap1b-deficient mice. Blood. 2008;111:2647-2656.
48. Voss AK, Gruss P, Thomas T. The guanine nucle-otide exchange factor C3G is necessary for the formation of focal adhesions and vascular maturation. Development. 2003;130:355-367.
49. Wei P, Satoh T, Edamatsu H, et al. Defective vascular morphogenesis and mid-gestation embryonic death in mice lacking RA-GEF-1. Biochem Biophys Res Commun. 2007;363:106-112.
50. Ohba Y, Ikuta K, Ogura A, et al. Requirement for C3G-dependent Rap1 activation for cell adhesion and embryogenesis. EMBO J. 2001;20:3333-3341.
51. Valles AM, Beuvin M, Boyer B. Activation of Rac1 by paxillin-Crk-DOCK180 signaling complex is antagonized by Rap1 in migrating NBT-II cells. J Biol Chem. 2004;279:44490-44496.
52. McLeod SJ, LiAH, Lee RL, Burgess AE, Gold MR. The Rap GTPases regulate B cell migration toward the chemokine stromal cell-derived factor-1 (CXCL12): potential role for Rap2 in promoting B cell migration. J Immunol. 2002;169:1365-1371.
53. Kinashi T. Intracellular signalling controlling integrin activation in lymphocytes. Nat Rev Immunol. 2005;5:546-559.
54. Kiosses WB, Shattil SJ, Pampori N, Schwartz MA. Rac recruits high-affinity integrin alphav-beta3 to lamellipodia in endothelial cell migration. Nat Cell Biol. 2001;3:316-320.
55. Arthur WT, Quilliam LA, Cooper JA. Rap1 promotes cell spreading by localizing Rac guanine nucleotide exchange factors. J Cell Biol. 2004; 167:111-122.
56. Schneller M, Vuori K, Ruoslahti E. Alphavbeta3 integrin associates with activated insulin and PDGFbeta receptors and potentiates the biological activity of PDGF. EMBO J. 1997;16:5600-5607.
57. Borges E, Jan Y, Ruoslahti E. Platelet-derived growth factor receptor beta and vascular endothelial growth factor receptor 2 bind to the beta 3 integrin through its extracellular domain. J Biol Chem. 2000;275:39867-39873.
58. EnomotoA, Murakami H, Asai N, et al. Akt/PKB regulates actin organization and cell motility via Girdin/APE. Dev Cell. 2005;9:389-402.
59. Li J, Ballif BA, Powelka AM, Dai J, Gygi SP, Hsu VW. Phosphorylation ofACAP1 byAkt regulates the stimulation-dependent recycling of integrin beta1 to control cell migration. Dev Cell. 2005;9: 663-673.
60. Somanath PR, Kandel ES, Hay N, Byzova TV. Akt1 signaling regulates integrin activation, matrix recognition, and fibronectin assembly. J Biol Chem. 2007;282:22964-22976.
61. Li S, Guan JL, Chien S. Biochemistry and biomechanics of cell motility. Annu Rev Biomed Eng. 2005;7:105-150.
62. Kinashi T, Katagiri K. Regulation of lymphocyte adhesion and migration by the small GTPase Rap1 and its effector molecule, RAPL. Immunol Lett. 2004;93:1-5.
63. Tohyama Y, Katagiri K, Pardi R, Lu C, Springer TA, Kinashi T. The critical cytoplasmic regions of the alphaL/beta2 integrin in Rap1-induced adhesion and migration. Mol Biol Cell. 2003;14:2570-2582.