β3 Integrin promotes long-lasting activation and polarization of vascular endothelial growth factor receptor 2 by immobilized ligand

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 35, Issue 10, 2015, Pages 2161-2171

  Ravelli, Cosetta ^a   Grillo, Elisabetta ^a   Corsini, Michela ^a   Coltrini, Daniela ^a   Presta, Marco ^a   Mitola, Stefania ^a  

^a UNIVERSITY OF BRESCIA   (Italy)

Author keywords

Angiogenesis; Gremlin; Integrins; Lipid rafts; VEGFR2

Indexed keywords

BETA3 INTEGRIN; BONE MORPHOGENETIC PROTEIN; FOCAL ADHESION KINASE; GREMLIN; IMMOBILIZED PROTEIN; INTEGRIN RECEPTOR; LIGAND; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG; VASCULOTROPIN RECEPTOR 2;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; FEMALE; FLUORESCENCE RESONANCE ENERGY TRANSFER; FOCAL ADHESION; GENE ACTIVATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; INTRACELLULAR SIGNALING; LIPID RAFT; POLARIZATION; PRIORITY JOURNAL; TIME-LAPSE VIDEO MICROSCOPY; WESTERN BLOTTING; ANGIOGENESIS; CELL CULTURE; CYTOLOGY; METABOLISM; PHYSIOLOGY; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM;

CELLS, CULTURED; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; INTEGRIN BETA3; NEOVASCULARIZATION, PHYSIOLOGIC; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84942234107     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.115.306230     Document Type: Article

References (40)

1. Carmeliet P, Jain RK. Angiogenesis in cancer and other diseases. Nature. 2000;407:249-257. doi: 10. 1038/35025220.
2. Rusnati M, Presta M. Extracellular angiogenic growth factor interactions: An angiogenesis interactome survey. Endothelium. 2006;13:93-111. doi: 10. 1080/10623320600698011.
3. Ferrara N. Binding to the extracellular matrix and proteolytic processing: two key mechanisms regulating vascular endothelial growth factor action. Mol Biol Cell. 2010;21:687-690. doi: 10. 1091/mbc. E09-07-0590.
4. Roy R, Zhang B, Moses MA. Making the cut: protease-mediated regulation of angiogenesis. Exp Cell Res. 2006;312:608-622. doi: 10. 1016/j. yexcr. 2005. 11. 022.
5. Tanghetti E, Ria R, Dell'Era P, Urbinati C, Rusnati M, Ennas MG, Presta M. Biological activity of substrate-bound basic fibroblast growth factor (FGF2): recruitment of FGF receptor-1 in endothelial cell adhesion contacts. Oncogene. 2002;21:3889-3897. doi: 10. 1038/sj. onc. 1205407.
6. Chen TT, Luque A, Lee S, Anderson SM, Segura T, Iruela-Arispe ML. Anchorage of VEGF to the extracellular matrix conveys differential signaling responses to endothelial cells. J Cell Biol. 2010;188:595-609. doi: 10. 1083/jcb. 200906044.
7. Hudson N, Powner MB, Sarker MH, Burgoyne T, Campbell M, Ockrim ZK, Martinelli R, Futter CE, Grant MB, Fraser PA, Shima DT, Greenwood J, Turowski P. Differential apicobasal VEGF signaling at vascular blood-neural barriers. Dev Cell. 2014;30:541-552. doi: 10. 1016/j. devcel. 2014. 06. 027.
8. Sneddon JB, Zhen HH, Montgomery K, van de Rijn M, Tward AD, West R, Gladstone H, Chang HY, Morganroth GS, Oro AE, Brown PO. Bone morphogenetic protein antagonist gremlin 1 is widely expressed by cancer-associated stromal cells and can promote tumor cell proliferation. Proc Natl Acad Sci U S A. 2006;103:14842-14847. doi: 10. 1073/ pnas. 0606857103.
9. Stabile H, Mitola S, Moroni E, Belleri M, Nicoli S, Coltrini D, Peri F, Pessi A, Orsatti L, Talamo F, Castronovo V, Waltregny D, Cotelli F, Ribatti D, Presta M. Bone morphogenic protein antagonist Drm/gremlin is a novel proangiogenic factor. Blood. 2007;109:1834-1840. doi: 10. 1182/ blood-2006-06-032276.
10. Chiodelli P, Mitola S, Ravelli C, Oreste P, Rusnati M, Presta M. Heparan sulfate proteoglycans mediate the angiogenic activity of the vascular endothelial growth factor receptor-2 agonist gremlin. Arterioscler Thromb Vasc Biol. 2011;31:e116-e127. doi: 10. 1161/ATVBAHA. 111. 235184.
11. Mitola S, Moroni E, Ravelli C, Andres G, Belleri M, Presta M. Angiopoietin-1 mediates the proangiogenic activity of the bone morphogenic protein antagonist Drm. Blood. 2008;112:1154-1157. doi: 10. 1182/ blood-2007-09-111450.
12. Mitola S, Ravelli C, Moroni E, Salvi V, Leali D, Ballmer-Hofer K, Zammataro L, Presta M. Gremlin is a novel agonist of the major proangiogenic receptor VEGFR2. Blood. 2010;116:3677-3680. doi: 10. 1182/ blood-2010-06-291930.
13. Maiolo D, Mitola S, Leali D, Oliviero G, Ravelli C, Bugatti A, Depero LE, Presta M, Bergese P. Role of nanomechanics in canonical and noncanonical pro-angiogenic ligand/VEGF receptor-2 activation. J Am Chem Soc. 2012;134:14573-14579. doi: 10. 1021/ja305816p.
14. Ravelli C, Mitola S, Corsini M, Presta M. Involvement of ?v?3 integrin in gremlin-induced angiogenesis. Angiogenesis. 2013;16:235-243. doi: 10. 1007/s10456-012-9309-6.
15. Corsini M, Moroni E, Ravelli C, Andrés G, Grillo E, Ali IH, Brazil DP, Presta M, Mitola S. Cyclic adenosine monophosphate-response elementbinding protein mediates the proangiogenic or proinflammatory activity of gremlin. Arterioscler Thromb Vasc Biol. 2014;34:136-145. doi: 10. 1161/ ATVBAHA. 113. 302517.
16. Hughes CS, Radan L, Betts D, Postovit LM, Lajoie GA. Proteomic analysis of extracellular matrices used in stem cell culture. Proteomics. 2011;11:3983-3991. doi: 10. 1002/pmic. 201100030.
17. Cattelino A, Albertinazzi C, Bossi M, Critchley DR, de Curtis I. A cellfree system to study regulation of focal adhesions and of the connected actin cytoskeleton. Mol Biol Cell. 1999;10:373-391. doi: 10. 1091/ mbc. 10. 2. 373.
18. 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. doi: 10. 1093/emboj/18. 4. 882.
19. Urbinati C, Ravelli C, Tanghetti E, Belleri M, Giacopuzzi E, Monti E, Presta M, Rusnati M. Substrate-immobilized HIV-1 Tat drives VEGFR2/?(v)?(3)-integrin complex formation and polarization in endothelial cells. Arterioscler Thromb Vasc Biol. 2012;32:e25-e34. doi: 10. 1161/ATVBAHA. 111. 242396.
20. Fletcher PA, Scriven DR, Schulson MN, Moore ED. Multi-image colocalization and its statistical significance. Biophys J. 2010;99:1996-2005. doi: 10. 1016/j. bpj. 2010. 07. 006.
21. Insel PA, Patel HH. Membrane rafts and caveolae in cardiovascular signaling. Curr Opin Nephrol Hypertens. 2009;18:50-56. doi: 10. 1097/ MNH. 0b013e3283186f82.
22. Echarri A, Muriel O, Del Pozo MA. Intracellular trafficking of raft/ caveolae domains: insights from integrin signaling. Semin Cell Dev Biol. 2007;18:627-637. doi: 10. 1016/j. semcdb. 2007. 08. 004.
23. Schulson MN, Scriven DR, Fletcher P, Moore ED. Couplons in rat atria form distinct subgroups defined by their molecular partners. J Cell Sci. 2011;124(pt 7):1167-1174. doi: 10. 1242/jcs. 080929.
24. Allen JA, Halverson-Tamboli RA, Rasenick MM. Lipid raft microdomains and neurotransmitter signalling. Nat Rev Neurosci. 2007;8:128-140. doi: 10. 1038/nrn2059.
25. Mahabeleshwar GH, Feng W, Reddy K, Plow EF, Byzova TV. Mechanisms of integrin-vascular endothelial growth factor receptor crossactivation in angiogenesis. Circ Res. 2007;101:570-580. doi: 10. 1161/ CIRCRESAHA. 107. 155655.
26. Urbinati C, Bugatti A, Giacca M, Schlaepfer D, Presta M, Rusnati M. Alpha(v)beta3-integrin-dependent activation of focal adhesion kinase mediates NF-kappaB activation and motogenic activity by HIV-1 Tat in endothelial cells. J Cell Sci. 2005;118(pt 17):3949-3958. doi: 10. 1242/ jcs. 02518.
27. Sieg DJ, Hauck CR, Schlaepfer DD. Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration. J Cell Sci. 1999;112(pt 16):2677-2691.
28. Finley SD, Popel AS. Effect of tumor microenvironment on tumor VEGF during anti-VEGF treatment: systems biology predictions. J Natl Cancer Inst. 2013;105:802-811. doi: 10. 1093/jnci/djt093.
29. Anderson SM, Chen TT, Iruela-Arispe ML, Segura T. The phosphorylation of vascular endothelial growth factor receptor-2 (VEGFR-2) by engineered surfaces with electrostatically or covalently immobilized VEGF. Biomaterials. 2009;30:4618-4628. doi: 10. 1016/j. biomaterials. 2009. 05. 030.
30. Yu LM, Wosnick JH, Shoichet MS. Miniaturized system of neurotrophin patterning for guided regeneration. J Neurosci Methods. 2008;171:253-263. doi: 10. 1016/j. jneumeth. 2008. 03. 023.
31. Fan VH, Tamama K, Au A, Littrell R, Richardson LB, Wright JW, Wells A, Griffith LG. Tethered epidermal growth factor provides a survival advantage to mesenchymal stem cells. Stem Cells. 2007;25:1241-1251. doi: 10. 1634/stemcells. 2006-0320.
32. Leclerc C, Brose C, Nouzé C, Leonard F, Majlessi L, Becker S, von Briesen H, Lo-Man R. Immobilized cytokines as biomaterials for manufacturing immune cell based vaccines. J Biomed Mater Res A. 2008;86:1033-1040. doi: 10. 1002/jbm. A. 31751.
33. Fukuhara S, Sako K, Minami T, Noda K, Kim HZ, Kodama T, Shibuya M, Takakura N, Koh GY, Mochizuki N. Differential function of Tie2 at cellcell contacts and cell-substratum contacts regulated by angiopoietin-1. Nat Cell Biol. 2008;10:513-526. doi: 10. 1038/ncb1714.
34. 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. doi: 10. 1074/jbc. M007040200.
35. Amano H, Ikeda W, Kawano S, Kajita M, Tamaru Y, Inoue N, Minami Y, Yamada A, Takai Y. Interaction and localization of Necl-5 and PDGF receptor beta at the leading edges of moving NIH3T3 cells: Implications for directional cell movement. Genes Cells. 2008;13:269-284. doi: 10. 1111/j. 1365-2443. 2008. 01167. x.
36. Labrecque L, Royal I, Surprenant DS, Patterson C, Gingras D, Béliveau R. Regulation of vascular endothelial growth factor receptor-2 activity by caveolin-1 and plasma membrane cholesterol. Mol Biol Cell. 2003;14:334-347. doi: 10. 1091/mbc. E02-07-0379.
37. Zhai J, Lin H, Nie Z, Wu J, Cañete-Soler R, Schlaepfer WW, Schlaepfer DD. Direct interaction of focal adhesion kinase with p190RhoGEF. J Biol Chem. 2003;278:24865-24873. doi: 10. 1074/jbc. M302381200.
38. Wang R, Bi J, Ampah KK, Ba X, Liu W, Zeng X. Lipid rafts control human melanoma cell migration by regulating focal adhesion disassembly. Biochim Biophys Acta. 2013;1833:3195-3205. doi: 10. 1016/j. bbamcr. 2013. 09. 007.
39. Chichili GR, Rodgers W. Cytoskeleton-membrane interactions in membrane raft structure. Cell Mol Life Sci. 2009;66:2319-2328. doi: 10. 1007/ s00018-009-0022-6.
40. Gaus K, Chklovskaia E, Fazekas de St Groth B, Jessup W, Harder T. Condensation of the plasma membrane at the site of T lymphocyte activation. J Cell Biol. 2005;171:121-131. doi: 10. 1083/jcb. 200505047.