Rap1 promotes VEGFR2 activation and angiogenesis by a mechanism involving integrin αvβ3

Blood

Volumn 118, Issue 7, 2011, Pages 2015-2026

  Lakshmikanthan, Sribalaji ^a   Sobczak, Magdalena ^a   Chun, Changzoon ^b   Henschel, Angela ^a   Dargatz, Jillian ^a   Ramchandran, Ramani ^b   Chrzanowska Wodnicka, Magdalena ^a  

^a BLOOD RESEARCH INSTITUTE   (United States)

^b MEDICAL COLLEGE OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RAP1 PROTEIN; RAP1A PROTEIN; RAP1B PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; VITRONECTIN RECEPTOR;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; IN VIVO STUDY; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM; ZEBRA FISH;

EID: 80051865329     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-04-349282     Document Type: Article

References (52)

1. Carmeliet P. Angiogenesis in life, disease and medicine. Nature. 2005;438(7070):932-936. (Pubitemid 43093958)
2. Millauer B., Wizigmann-Voos S., Schnürch H., et al. High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell. 1993;72(6):835-846. (Pubitemid 23110226)
3. Shalaby F., Rossant J., Yamaguchi T.P., et al. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature. 1995;376(6535):62-66.
4. Zachary I., Gliki G. Signaling transduction mechanisms mediating biologic actions of the vascular endothelial growth factor family. Cardiovasc Res. 2001;49(3):568-581. (Pubitemid 32146420)
5. Ferrara N., Mass R.D., Campa C., Kim R. Targeting VEGF-A to treat cancer and age-related macular degeneration. Annu Rev Med. 2007;58(1):491-504. (Pubitemid 46706529)
6. Legate K.R., Wickstrom S.A., Fassler R. Genetic and cell biologic analysis of integrin outside-in signaling. Genes Dev. 2009;23(4):397-418.
7. Avraamides C.J., Garmy-Susini B., Varner J.A. Integrins in angiogenesis and lymphangiogenesis. Nat Rev Cancer. 2008;8(8):604-617.
8. Hynes R.O. Cell-matrix adhesion in vascular development. J Thromb Haemost. 2007;5(s1):32-40. (Pubitemid 46964284)
9. Brooks P.C., Clark R.A., Cheresh D.A. Requirement of vascular integrin [alpha]v[beta]3 for angiogenesis. Science. 1994;264:569-571.
10. Somanath P.R., Malinin N.L., Byzova T.V. Cooperation between integrin alpha(V)beta(3) and VEGFR2 in angiogenesis. Angiogenesis. 2009;12(2):177-185.
11. Soldi R., Mitola S., Strasly M., Defilippi P., Tarone G., Bussolino F. Role of alpha (v) beta(3) integrin in the activation of vascular endothelial growth factor receptor-2. EMBO J. 1999;18(4):882-892. (Pubitemid 29082268)
12. Mahabeleshwar G.H., Feng W.Y., Phillips D.R., Byzova T.V. Integrin signaling is critical for pathologic angiogenesis. J Exp Med. 2006;203(11):2495-2507. (Pubitemid 44664619)
13. Masson-Gadais B., Houle F., Laferriere J., Huot J. Integrin alpha (v) beta(3) requirement for VEGFR2-mediated activation of SAPK2/p38 and for Hsp90-dependent phosphorylation of focal adhesion kinase in endothelial cells activated by VEGF. Cell Stress Chaperones. 2003;8(1):37-52. (Pubitemid 36444089)
14. Mahabeleshwar G.H., FengW., Reddy K., Plow E.F., Byzova T.V. Mechanisms of integrin vascular endothelial growth factor receptor cross-activation in angiogenesis. Circ Res. 2007;101(6):570-580. (Pubitemid 351325874)
15. Caron E. Cellular functions of the Rap1 GTP-binding protein: A pattern emerges. J Cell Sci. 2003;116(3):435-440. (Pubitemid 36231283)
16. Boettner B., Van Aelst L. Control of cell adhesion dynamics by Rap1 signaling. Curr Opin Cell Biol. 2009;21(5):684-693.
17. Yan J.L., Li F., Ingram D.A., Quilliam L.A. Rap1a is a key regulator of fibroblast growth factor 2-induced angiogenesis and together with Rap1b controls human endothelial cell functions. Mol Cell Biol. 2008;28(18):5803-5810.
18. Chrzanowska-Wodnicka M., Kraus A.E., Gale D., White G.C., II, VanSluys J. Defective angiogenesis, endothelial migration, proliferation, and MAPK signaling in Rap1b-deficient mice. Blood. 2008;111(5):2647-2656.
19. Carmona G., Gottig S., Orlandi A., et al. Role of the small GTPase Rap1 for integrin activity regulation in endothelial cells and angiogenesis. Blood. 2009;113(2):488-497.
20. Chrzanowska-Wodnicka M. Regulation of angiogenesis by a small GTPase Rap1. Vasc Pharmacol. 2010;53(1-2):1-10.
21. Chrzanowska-Wodnicka M., Smyth S.S., Schoenwaelder S.M., Fischer T.H., White G.C. Rap1b is required for normal platelet function and hemostasis in mice. J Clin Invest. 2005;115(8):2296-2296.
22. Pan B-X, Vautier F., Ito W., Bolshakov V.Y., Morozov A. Enhanced cortico-amygdala efficacy and suppressed fear in absence of Rap1. J Neurosci. 2008;28(9):2089-2098. (Pubitemid 351317620)
23. Koni P.A., Joshi S.K., Temann U-A, Olson D., Burkly L., Flavell R.A. Conditional vascular cell adhesion molecule 1 deletion in mice: Impaired lymphocyte migration to bone marrow. J Exp Med. 2001;193(6):741-754.
24. Hodivala-Dilke K.M., McHugh K.P., Tsakiris D.A., et al. β3-integrin-deficient mice are a model for Glanzmann thrombasthenia showing placental defects and reduced survival. J Clin Invest. 1999;103(2):229-238. (Pubitemid 29053141)
25. Westerfield M. The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish. 4th ed. Eugene, OR: University of Oregon Press; 2000:2.1-2.2 chapter 2.0 "Breeding."
26. Kimmel B.E., Heberlein U., Rubin G.M. The homeo domain protein rough is expressed in a subset of cells in the developing Drosophila eye where it can specify photoreceptor cell subtype. Genes Dev. 1990;4:712-727.
27. Akhtar N., Dickerson E., Auerbach R. The sponge/Matrigel angiogenesis assay. Angiogenesis. 2002;5(1):75-80. (Pubitemid 36076925)
28. Sobczak M., Dargatz J., Chrzanowska-Wodnicka M. Isolation and culture of pulmonary endothelial cells from neonatal mice. J Vis Exp. 2010;46. pii:2316.
29. Gore A.V., Lampugnani M.G., Dye L., Dejana E., Weinstein B.M. Combinatorial interaction between CCM pathway genes precipitates hemorrhagic stroke. Dis Models Mech. 2008;1(4-5):275-281.
30. Bedell V.M., Yeo S.Y., Park K.W., et al. roundabout4 is essential for angiogenesis in vivo. Proc Natl Acad Sci U S A. 2005;102(18):6373-6378. (Pubitemid 40617450)
31. Takakura N., Huang X-L, Naruse T., et al. Critical role of the TIE2 endothelial cell receptor in the development of definitive hematopoiesis. Immunity. 1998;9(5):677-686. (Pubitemid 28557596)
32. Uemura A., Kusuhara S., Katsuta H., Nishikawa S-I. Angiogenesis in the mouse retina: A model system for experimental manipulation. Exp Cell Res. 2006;312(5):676-683. (Pubitemid 43290344)
33. Gerhardt H., Betsholtz C. Endothelial-pericyte interactions in angiogenesis. Cell Tissue Res. 2003;314(1):15-23. (Pubitemid 37409909)
34. Somanath P.R., Ciocea A., Byzova T.V. Integrin and growth factor receptor alliance in angiogenesis. Cell Biochem Biophys. 2009;53(2):53-64.
35. Yang J.T., Rayburn H., Hynes R.O. Embryonic mesodermal defects in [alpha]5 integrin-deficient mice. Development. 1993;119:1093-1105. (Pubitemid 23358579)
36. Koistinen P., Heino J. The selective regulation of (alpha)v(beta)1 integrin expression is based on the hierarchical formation of αV-containing heterodimers. J Biol Chem. 2002;277(27):24835-24841.
37. Mahabeleshwar G.H., Chen J.H., Feng W.Y., Somanath P.R., Razorenova O.V., Byzova T.V. Integrin affinity modulation in angiogenesis. Cell Cycle. 2008;7(3):335-347. (Pubitemid 351366497)
38. Stork P.J.S., Dillon T.J. Multiple roles of Rap1 in hematopoietic cells: Complementary versus antagonistic functions. Blood. 2005;106(9):2952-2961. (Pubitemid 41565885)
39. Isogai S., Lawson N.D., Torrealday S., Horiguchi M., Weinstein B.M. Angiogenic network formation in the developing vertebrate trunk. Development. 2003;130(21):5281-5290. (Pubitemid 37369685)
40. Chan J., Bayliss P.E., Wood J.M., Roberts T.M. Dissection of angiogenic signaling in zebrafish using a chemical genetic approach. Cancer Cell. 2002;1(3):257-267. (Pubitemid 41039150)
41. Cross L.M., Cook M.A., Lin S., Chen J-N, Rubinstein A.L. Rapid analysis of angiogenesis drugs in a live fluorescent zebrafish assay. Arterioscler Thromb Vasc Biol. 2003;23(5):911-912. (Pubitemid 36566186)
42. Gerhardt H. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol. 2003;161:1163-1177. (Pubitemid 36870177)
43. Asuri S., Yan J.L., Paranavitana N.C., Quilliam L.A. E-cadherin dis-engagement activates the Rap1 GTPase. J Cell Biochem. 2008;105(4):1027-1037.
44. Balzac F., Avolio M., Degani S., et al. E-cadherin endocytosis regulates the activity of Rap1: A traffic light GTPase at the crossroads between cadherin and integrin function. J Cell Sci. 2005;118(20):4765-4783. (Pubitemid 41646386)
45. Lafuente E.M., Van Puijenbroek A.A.F.L., Krause M., et al. RIAM, an Ena/VASP and profilin ligand, interacts with Rap1-GTP and mediates Rap1-induced adhesion. Dev Cell. 2004;7(4):585-595. (Pubitemid 39341843)
46. Lee H-S, Lim C.J., Puzon-McLaughlin W., Shattil S.J., Ginsberg M.H. RIAM Activates Integrins by linking talin to Ras GTPase membrane-targeting sequences. J Biol Chem. 2009;284(8):5119-5127.
47. Abid M.R., Spokes K.C., Shih S.C., Aird W.C. NADPH oxidase activity selectively modulates vascular endothelial growth factor signaling pathways. J Biol Chem. 2007;282(48):35373-35385. (Pubitemid 350232487)
48. Garrido-Urbani S., Jemelin S., Deffert C., et al. Targeting vascular NADPH oxidase 1 blocks tumor angiogenesis through a PPAR alpha mediated mechanism. PLoS ONE. 2011;6(2).
49. Nasevicius A., Larson J., Ekker S.C. Distinct requirements for zebrafish angiogenesis revealed by a VEGF-A morphant. Yeast. 2000;17(4):294-301. (Pubitemid 32051422)
50. Pannekoek W.J., Kooistra M.R.H., Zwartkruis F.J.T., Bos J.L. Cell-cell junction formation: The role of Rap1 and Rap1 guanine nucleotide exchange factors. Biochim Biophys Acta. Biomembranes. 2009;1788(4):790-796.
51. Hong J., Doebele R.C., Lingen M.W., Quilliam L.A., Tang W-J, Rosner M.R. Anthrax edema toxin inhibits endothelial cell chemotaxis via Epac and Rap1. J Biol Chem. 2007;282(27):19781-19787. (Pubitemid 47100121)
52. Doebele R.C., Schulze-Hoepfner F.T., Hong J., et al. Anovel interplay between Epac/Rap1 and mitogen-activated protein kinase kinase 5/extracellular signal-regulated kinase 5 (MEK5/ERK5) regulates thrombospondin to control angiogenesis. Blood. 2009;114(20):4592-4600.