Differential uPAR recruitment in caveolar-lipid rafts by GM1 and GM3 gangliosides regulates endothelial progenitor cells angiogenesis

Journal of Cellular and Molecular Medicine

Volumn 19, Issue 1, 2015, Pages 113-123

  Margheri, Francesca ^a   Papucci, Laura ^a   Schiavone, Nicola ^a   D'Agostino, Riccardo ^a,b   Trigari, Silvana ^b   Serratì, Simona ^a   Laurenzana, Anna ^a   Biagioni, Alessio ^a   Luciani, Cristina ^a   Chillà, Anastasia ^a   Andreucci, Elena ^a   Del Rosso, Tommaso ^c   Margheri, Giancarlo ^b   Del Rosso, Mario ^b,d   Fibbi, Gabriella ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b CNR   (Italy)

^c PONTIFICAL CATHOLIC UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^d ISTITUTO TOSCANO TUMORI   (Italy)

Author keywords

Angiogenesis; Caveolar lipid rafts; Endothelial colony forming cells; Endothelial progenitor cells; GM1; GM3; Lipid rafts; MAPKinases; UPAR

Indexed keywords

CAVEOLIN 1; GANGLIOSIDE GM1; GANGLIOSIDE GM3; UROKINASE RECEPTOR;

ANGIOGENESIS; CAVEOLA; CELL MEMBRANE; CFU COUNTING; DRUG EFFECTS; ENDOTHELIAL PROGENITOR CELL; HUMAN; KINETICS; METABOLISM; NEWBORN; PHENOTYPE; SIGNAL TRANSDUCTION;

CAVEOLAE; CAVEOLIN 1; COLONY-FORMING UNITS ASSAY; ENDOTHELIAL PROGENITOR CELLS; G(M1) GANGLIOSIDE; G(M3) GANGLIOSIDE; HUMANS; INFANT, NEWBORN; KINETICS; MEMBRANE MICRODOMAINS; NEOVASCULARIZATION, PHYSIOLOGIC; PHENOTYPE; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; SIGNAL TRANSDUCTION;

EID: 84921514492     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/jcmm.12410     Document Type: Article

References (34)

1. Pike LJ. The challenge of lipid rafts. J Lipid Res. 2008; 50: S323.
2. Sonderfeld S, Conzelman E, Schwarzmann G, et al. Incorporation and metabolism of ganglioside GM2 in skin fibroblasts from normal and GM2 gangliosidosis subjects. Eur J Biochem. 1985; 149: 247-55.
3. Birklé S, Zebg G, Gao L, et al. Role of tumor-associated gangliosides in cancer progression. Biochimie. 2003; 85: 455-63.
4. De Cristian G, Morbidelli L, Alessandri G, et al. Synergism between, gangliosides and basic fibroblast growth factor in favouring survival, growth, and motility of capillary endothelium. J Cell Physiol. 1990; 144: 505-10.
5. Koochekpour S, Merzak A, Pilkington GJ. Vascular endothelial growth factor production is stimulated by gangliosides and tgf-beta isoforms in human glioma cells in vitro. Cancer Lett. 1996; 102: 209-15.
6. Ziche M, Morbidelli L, Alessandri G, et al. Angiogenesis can be stimulated or repressed in vivo by a change in GM3:GD3 ganglioside ratio. Lab Invest. 1992; 67: 711-5.
7. Slevin M, Kumar S, He X, et al. Physiological concentrations of gangliosides GM1, GM2 and GM3 differentially modify basic-fibroblast-growth-factor-induced mitogenesis and the associated signalling pathway in endothelial cells. Int J Cancer. 1999; 82: 412-23.
8. Cunningham O, Andolfo A, Santovito ML, et al. Dimerization controls the lipid raft partitioning of uPAR/CD87 and regulates its biological functions. EMBO J. 2003; 22: 5994-6003.
9. Margheri F, Chillà A, Laurenzana A, et al. Endothelial progenitor cell-dependent angiogenesis requires localization of the full-length form of uPAR in caveolae. Blood. 2011; 118: 3743-55.
10. Rao JS, Gujrati M, Chetty C. Tumor-associated soluble uPAR-directed endothelial cell motility and tumor angiogenesis. Oncogenesis. 2013; 2: e53.
11. Mao Y, Tero R, Imai Y, et al. The morphology of GM1x/SM0.6-x/Chol0.4 planar bilayers supported on SiO2 surfaces. Chem Phys Lett. 2008; 460: 289-94.
12. Margheri G, D'Agostino R, Trigari S, et al. The β-Subunit of Cholera Toxin has a high affinity for ganglioside GM1 in solid supported lipid membranes with a lipid raft-like composition. Lipids. 2014; 49: 203-6.
13. 2 plasmonic substrates. Lipids. 2013; 48: 739-47.
14. Simons K, Toomre D. Lipid rafts and signal transduction. Nat Rev Mol Cell Biol. 2000; 1: 31-9. Review. Erratum in: Nat Rev Mol Cell Biol 2001; 2:216.
15. Binder VH, Barragan V, Menger FM. Domains and rafts in lipid membranes. Angew Chem Int Ed Engl. 2003; 42: 5802-27.
16. Chillà A, Magherini F, Margheri F, et al. Proteomic identification of VEGF-dependent protein enrichment to membrane caveolar-raft microdomains in endothelial progenitor cells. Mol Cell Proteomics. 2013; 12: 1926-38.
17. Margheri F, Schiavone N, Papucci L, et al. GDF5 regulates TGFß-dependent angiogenesis in breast carcinoma MCF-7 cells: in vitro and in vivo control by anti-TGFß peptides. PLoS ONE. 2012; 7: e50342.
18. Margheri F, Manetti M, Serrati S, et al. Domain 1 of the urokinase-type plasminogen activator receptor is required for its morphologic and functional, beta2 integrin-mediated connection with actin cytoskeleton in human microvascular endothelial cells: failure of association in systemic sclerosis endothelial cells. Arthritis Rheum. 2006; 54: 3926-38.
19. Bolte S, Cordelieres FP. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc. 2006; 224: 213-32.
20. Edwards PR, Lowe PA, Leatherbarrow RJ. Ligand loading at the surface of an optical biosensor and its effect upon the kinetics of protein-protein interactions. J Mol Recognit. 1997; 10: 128-34.
21. Eden G, Archinti M, Furlan F, et al. The urokinase receptor interactome. Curr Pharm Des. 2011; 17: 1874-89.
22. Brunner PM, Heier PC, Mihaly-Bison J, et al. Density enhanced phosphatase-1 down-regulates urokinase receptor surface expression in confluent endothelial cells. Blood. 2011; 117: 4154-61.
23. Lajoie P, Kojic LD, Nim S, et al. Caveolin-1 regulation of dynamin-dependent, raft-mediated endocytosis of cholera toxin-B sub-unit occurs independently of caveolae. J Cell Mol Med. 2009; 13: 3218-25.
24. Chen Y, Qin J, Chen ZW. Fluorescence-topographic NSOM directly visualizes peak-valley polarities of GM1/GM3 rafts in cell membrane fluctuations. J Lipid Res. 2008; 49: 2268-75.
25. Li Calzi S, Neu MB, Shaw LC, et al. EPCs and pathological angiogenesis: when good cells go bad. Microvasc Res. 2010; 79: 207-16.
26. Sahores M, Prinetti A, Chiabrando G, et al. uPA binding increases UPAR localization to lipid rafts and modifies the receptor microdomain composition. Biochim Biophys Acta. 2008; 1778: 250-9.
27. Kiyan J, Smith G, Haller H, et al. Urokinase-receptor-mediated phenotypic changes in vascular smooth muscle cells require the involvement of membrane rafts. Biochem J. 2009; 423: 343-51.
28. Frank PG, Woodman SE, Park DS, et al. Caveolin, caveolae, and endothelial cell function. Arterioscler Thromb Vasc Biol. 2003; 23: 1161-8.
29. Liao WX, Feng L, Zhang H, et al. Compartmentalizing VEGF-induced ERK2/1 signaling in placental artery endothelial cell caveolae: a paradoxical role of caveolin-1 in placental angiogenesis in vitro. Mol Endocrinol. 2009; 23: 1428-44.
30. Poettler M, Unseld M, Mihaly-Bison J, et al. The urokinase receptor (CD87) represents a central mediator of growth factor-induced endothelial cell migration. Thromb Haemost. 2012; 108: 357-66.
31. Deng W, Li R, Ladisch S. Influence of cellular ganglioside depletion on tumor formation. J Natl Cancer Inst. 2000; 92: 912-7.
32. Prinetti A, Aureli M, Illuzzi G, et al. GM3 synthase overexpression results in reduced cell motility and in caveolin-1 upregulation in human ovarian carcinoma cells. Glycobiology. 2010; 20: 62-77.
33. Fuentes R, Allman R, Mason MD. Ganglioside expression in lung cancer cell lines. Lung Cancer. 1997; 18: 21-33.
34. Cortese K, Sahores M, Madsen CD, et al. Clathrin and LRP-1-independent constitutive endocytosis and recycling of uPAR. PLoS ONE. 2008; 3: e3730.