Endoglin overexpression modulates cellular morphology, migration, and adhesion of mouse fibroblasts

European Journal of Cell Biology

Volumn 78, Issue 9, 1999, Pages 614-623

  Guerrero Esteo, Mercedes ^a   Lastres, Pedro ^a   Letamendía, Ainhoa ^a   Pérez Alvarez, María José ^b   Langa, Carmen ^a   López, Luis A ^c   Fabra, Angels ^c   García Pardo, Angeles ^a   Vera, Sonia ^d   Letarte, Michelle ^d   Bernabéu, Carmelo ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c HOSPITAL DURAN I REYNALS   (Spain)

^d HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

Endoglin; Fibroblasts; HHT; TGF ; Transfectants

Indexed keywords

ARGINYLGLYCYLASPARTIC ACID; ENDOGLIN; FIBRONECTIN; INTEGRIN; LAMININ; PLASMINOGEN ACTIVATOR INHIBITOR 1; POLYCLONAL ANTIBODY;

ANIMAL CELL; ARTICLE; CELL ADHESION; CELL MIGRATION; CELL STRUCTURE; CHEMOTAXIS; CONTROLLED STUDY; DNA TRANSFECTION; FIBROBLAST; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN SYNTHESIS; WOUND HEALING;

ANIMALIA; EUKARYOTA;

EID: 0032871898     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0171-9335(99)80046-6     Document Type: Article

References (62)

1. Adam, P. J., G. J. Clesham, P. L. Weissberg (1998): Expression of endoglin mRNA and protein in human vascular smooth muscle cells. Biochem. Biophys. Res. Commun. 247, 33-37.
2. Akiyama, S. K., K. M. Yamada (1987): Biosynthesis and acquisition of biological activity of the fibronectin receptor. J. Biol. Chem. 262, 17536-17542.
3. Attisano, L., J. Carcamo, F. Ventura, F. M. B. Weis, J. Massagué, J. L. Wrana (1993): Identification of human activin and TGF-β type I receptors that form heteromeric kinase complexes with type II receptors. Cell 75, 671-680.
4. Barbara, N. P., J. L. Wrana, M. Letarte (1999): Endoglin is an accessory protein that interacts with the signalling receptor complex of multiple members of the TGF-β superfamily. J. Biol. Chem. 274, 584-594.
5. Belloβn, T., A. Corbí, P. Lastres, C. Calés, M. Cebrián, S. Vera, S. Cheifetz, J. Massagué, M. Letarte, C. Bernabéu (1993): Identification and expression of two forms of the human transforming growth factor-β-binding protein endoglin with distinct cytoplasmic regions. Eur. J. Immunol. 23, 2340-2345.
6. Böttinger, E. P., J. J. Letterio, A. B. Roberts (1997): Biology of TGF-β in knockout and transgenic mouse models. Kidney Int. 51, 1355-1360.
7. Braverman, I. M., A. Keh, B. S. Jacobson (1990): Ultrastructure and three-dimensional organization of the telangiectases of hereditary hemorrhagic telangiectasia. J. Invest. Dermatol. 95, 422-427.
8. Caniggia, I., C. V. Taylor, J. W. Knox Ritchie, S. J. Lye, M. Letarte (1997): Endoglin regulates trophoblast differentiation along the invasive pathway in human placental villous explants. Endocrinology 138, 4977-4988.
9. Chavakis, T., S. M. Kanse, B. Yutzy, H. R. Lijnen, K. T. Preissner (1998): Vitronectin concentrates proteolytic activity on the cell surface and extracellular matrix by trapping soluble urokinase receptor-urokinase complexes. Blood 91, 2305-2312.
10. Cheifetz, S., T. Bellón, C. Calés, S. Vera, C. Bernabéu, J. Massagué, M. Letarte (1992): Endoglin is a component of the transforming growth factor-α receptor system in human endothelial cells. J. Biol. Chem. 267, 19027-19030.
11. Chen, W. C., B. Obrink (1991): Cell-cell contacts mediated by E-cadherin (uvomorulin) restrict invasive behavior of L-cells. J. Cell Biol. 114, 319-327.
12. Corbett, S. A., C. L. Wilson, J. E. Schwarzbauer (1996): Changes in cell spreading and cytoskeletal organization are induced by adhesion to a fibronectin-fibrin matrix. Blood 88, 158-166.
13. Corbí, A. (1996): Leukocyte Integrins: Structure, Expression and Function. R. G. Landes Series in Molecular Biology Intelligence Unit, Springer-Verlag, Heidelberg, Germany.
14. Fernández-Ruiz, E., S. St-Jacques, T. Bellón, M. Letarte, C. Bernabéu (1993): Assignment of the human endoglin gene (END) to chromosome 9q34-qter. Cytogenet. Cell Genet. 64, 204-207.
15. Ge, A. Z., E. C. Butcher (1994): Cloning and expression of a cDNA encoding mouse endoglin, an endothelial cell TGF-β ligand. Gene 138, 201-206.
16. Gougos, A., M. Letarte (1988): Identification of a human endothelial cell antigen with monoclonal antibody 44G4 produced against a pre-B leukemic cell line. J. Immunol. 141, 1925-1933.
17. Gougos, A., M. Letarte (1990): Primary structure of endoglin, an RGD-containing glycoprotein of human endothelial cells. J. Biol. Chem. 265, 8361-8364.
18. Gougos, A., S. St-Jacques, A. Greaves, P. J. O'Connell, A. J. F. d'Apice, H. J. Bühring, C. Bernabéu, J. A. van Mourik, M. Letarte (1992): Identification of distinct epitopes of endoglin, an RGD-containing glycoprotein of endothelial cells, leukemic cells, and syncytiotrophoblasts. Int. Immunol. 4, 83-92.
19. Gutmacher, A. E., D. A. Marchuk, R. I. White Jr. (1995): Hereditary hemorrhagic telangiectasia. New Engl. J. Med. 333, 918-924.
20. Horwitz A., K. Duggan, C. Buck, M. C. Beckerle, K. Burridge (1986): Interaction of plasma membrane fibronectin receptor with talin - a transmembrane linkage. Nature 320, 531-533.
21. Hynes, R. O. (1990): Fibronectins. Springer Series in Molecular Biology. (ed. A. Rich), Springer-Verlag, New York.
22. Ignotz, R. A., J. Massagué (1986): Transforming growth factor-β stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix. J. Biol. Chem. 261, 4337-4345.
23. Kano, Y., K. Katoh, M. Masuda, K. Fijiwara (1996): Macromolecular composition of stress fiber-plasma membrane attachment sites in endothelial cells in situ. Circ. Res. 79, 1000-1006.
24. Kwaan, H. C., S. Silverman (1973): Fibrinolytic activity in lesions of hereditary hemorrhagic telangiectasia. Arch. Dermatol. 107, 571-573.
25. Laiho, M., L. Ronnstrand, J. Heino, J. A. Decaprio, J. W. Ludlow, D. M. Livingston, J. Massagué (1991): Control of JunB and extracellular matrix protein expression by transforming growth factor-β1 is independent of SV40 T antigen-sensitive growth inhibitory events. Mol. Cell. Biol. 11, 972-978.
26. Lastres, P., T. Bellón, C. Cabañas, F. Sánchez-Madrid, A. Acevedo, A. Gougos, M. Letarte, C. Bernabéu (1992): Regulated expression on human macrophages of endoglin, an Arg-Gly-Asp-containing surface antigen. Eur. J. Immunol. 22, 393-397.
27. Lastres, P., A. Letamendía, H. Zhang, C. Rius, N. Almendro, U. Raab, L. A. López, C. Langa, A. Fabra, M. Letarte, C. Bernabéu (1996): Endoglin modulates cellular responses to TGF-β1. J. Cell Biol. 133, 1109-1121.
28. Lastres, P., J. Martín-Pérez, C. Langa, C. Bernabéu (1994): Phosphorylation of the human-transforming-growth-factor-β-binding protein endoglin. Biochem. J. 301, 765-768.
29. Lauffenburger, D. A., A. F. Horwitz (1996): Cell migration: a physically integrated molecular process. Cell 84, 359-369.
30. Lawrence, D. A., S. Palaniappan, S. Stefansson, S. T. Olson, A. M. Francis-Chmura, J. D. Shore, D. Ginsburg (1997): Characterization of the binding of different conformational forms of plasminogen activator inhibitor-1 to vitronectin. Implications for the regulation of pericellular proteolysis. J. Biol. Chem. 272, 7676-7680.
31. Lenter, M., H. Uhlig, A. Hamann, P. Jenö, B. Imhof, D. Vestweber (1993): A monoclonal antibody against an activation epitope on mouse integral chain β1 blocks adhesion of lymphocytes to the endothelial integrin α6β1. Proc. Natl. Acad. Sci. USA 90, 9051-9055.
32. Letamendía, A., P. Lastres, L. M. Botella, U. Raab, C. Langa, B. Velasco, L. Attisano, C. Bernabéu (1998): Role of endoglin in cellular responses to transforming growth factor-β. A comparative study with betaglycan. J. Biol. Chem. 273, 33011-33019.
33. Llorens, A., A. Vinyals, P. Alia, L. López-Barcons, M. Gonzalez-Garrigues, A. Fabra (1997): Metastatic ability of MXT mouse mammary subpopulations correlates with clonal expression and/ or membrane-association of gelatinase A. Mol. Carcinog. 19, 54-66.
34. MacAllister, K. A., K. M. Grogg, D. W. Johnson, C. J. Gallione, M. A. Baldwin, C. E. Jackson, E. A. Helmbold, D. S. Markel, W. C. McKinnon, J. Murrell, M. K. McCormick, M. A. Pericak-Vance, P. Heutink, B. A. Oostra, T. Haitjema, C. J. J. Westerman, M. E. Porteus, A. E. Guttmacher, M. Letarte, D. A. Marchuk (1994): Endoglin, a TGF-β binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nature Genet. 8, 345-351.
35. Macías-Silva, M., P. A. Hoodless, S. J. Tang, M. Buchwald, J. L. Wrana (1998): Specific activation of Smad1 signalling pathways by the BMP7 type I receptor, ALK2. J. Biol. Chem. 273, 25628-25636.
36. Marchuk, D. A. (1998): Genetic abnormalities in hereditary hemorrhagic telangiectasia. Curr. Opin. Hematol. 5, 332-338.
37. Massagué, J. (1990): The transforming growth factor-β family. Annu. Rev. Cell Biol. 6, 597-641.
38. O'Connell, P. J., A. Mckenzie, N. Fisicaro, S. P. Rockman, M. J. Pearse, A. J. F. d'Apice (1992): Endoglin: a 180-kD endothelial cell and macrophage restricted differentiation molecule. Clin. Exp. Immunol. 90, 154-159.
39. Pece, N., S. Vera, U. Cymerman, R. I. White, J. L. Wrana, M. Letarte (1997): Mutant endoglin in hereditary hemorrhagic telangiectasia type 1 is transiently expressed intracellularly and is not a dominant negative. J. Clin. Invest. 100, 2568-2579.
40. Pepper, M. S. (1997): Transforming growth factor-beta: Vasculogenesis, angiogenesis, and vessel wall integrity. Cytokine Growth Factor Rev. 8, 21-43.
41. Piantanida, M., E. Buscarini, C. Dellavecchia, A. Minelli, A. Rossi, L. Buscarini, C. Danesino (1997): Hereditary haemorrhagic telangiectasia with extensive liver involvement is not caused by either HHT1 or HHT2. J. Med. Genet. 33, 444-443.
42. Pichuantes S., S. Vera, A. Bourdeau, N. Pece, S. Kumar, E. A. Wayner, M. Letarte (1997): Mapping epitopes to distinct regions of the extracellular domain of endoglin using bacterially expressed recombinant fragments. Tissue Antigens 50, 265-276.
43. Pintavorn, P., B. J. Ballermann (1997): TGF-β and the endothelium during immune injury. Kidney Int. 51, 1401-1412.
44. Planus, E., G. Barlovatz-Meimon, R. A. Rogers, S. Bonavaud, D. E. Ingber, N. Wang (1997): Binding of urokinase to plasminogen activator inhibitor type-1 mediates cell adhesion and spreading. J. Cell Sci. 110, 1091-1098.
45. Preissner, K. T., A. E. May, A. E. Wohn, M. Germer, S. M. Kanse (1997): Molecular crosstalk between adhesion receptors and proteolytic cascades in vascular remodelling. Thromb. Haemostasis 78, 88-95.
46. Qu, R., M. Silver, M. Letarte (1998): Distribution of endoglin in human development reveals high levels on endocardial cushion tissue mesenchyme during valve formation. Cell Tissue Res. 292, 333-343.
47. Roberts, A. B., M. B. Sporn (1993): Physiological actions and clinical applications of transforming growth factor-β (TGF-β). Growth Factors 8, 1-9.
48. Robledo, M. M., A. Hidalgo, P. Lastres, A. G. Arroyo, C. Bernabéu, F. Sánchez-Madrid, J. Teixidó (1996): Characterization of TGF-β binding proteins in human bone marrow stromal cells. Brit. J. Haematol. 93, 507-514.
49. Rokhlin, O. W., M. B. Cohen, H. Kubagawa, M. Letarte, M. D. Cooper (1995): Differential expression of endoglin on fetal and adult hematopoietic cells in human bone marrow. J. Immunol. 154, 4456-4465.
50. Ruoslahti, E., E. Engvall (1997): Integrins and vascular extracellular matrix assembly. J. Clin. Invest. 100 (Suppl), S53-S56.
51. Saba, H. I., G. A. Morelli, L. A. Logrono (1994): Treatment of bleeding in hereditary hemorrhagic telangiectasia with aminocaproic acid. New Engl. J. Med. 330, 1789-1790.
52. Sánchez-Aparicio, P., C. Domínguez-Jiménez, A. García-Pardo (1994): Activation of the α4β1 integrin through the β1 subunit induces recognition of the RGD sequence in fibronectin. J. Cell Biol. 126, 271-279.
53. Schimmenti L. A., H. C. Yan, J. A. Madri, S. M. Albelda (1992): Platelet endothelial cell adhesion molecule, PECAM-1, modulates cell migration. J. Cell. Physiol. 153, 417-428.
54. Shen, C. X., S. Stewart, E. Wayner, W. Carter, J. Wilkins (1991): Antibodies to different members of the beta 1 (CD29) integrins induce homotypic and heterotypic cellular aggregation. Cell. Immunol. 138, 216-228.
55. Shovlin, C. L. (1997): Molecular defects in rare bleeding disorders: Hereditary haemorrhagic telangiectasia. Thromb. Haemostasis 78, 145-150.
56. St-Jacques, S., U. Cymerman, N. Pece, M. Letarte (1994): Molecular characterization and in situ localization of murine endoglin reveal that it is a transforming growth factor-β binding protein of endothelial and stromal cells. Endocrinology 134, 2645-2657.
57. Sugimoto, K., S. Fuji, T. Takemasa, K. Yamashita (1997): Factors inducing codistribution of marginal actin fibers and fibronectin in rat aortic endothelial cells. Am. J. Physiol. 272, H2188-2194.
58. Ten Dijke, P., H. Yamashita, H. Ichijo, P. Franzen, M. Laiho, K. Miyazono, C.-H. Heldin (1994): Characterization of type 1 receptors for transforming growth factor-β and activin. Science 264, 101-104.
59. Thalacker, F. W., M. Nilsen-Hamilton (1987): Specific induction of secreted proteins by transforming growth factor-β and 12-O-tetradecanoylphorbol-13-acetate. J. Biol. Chem. 262, 2283-2290.
60. Waltz, D. A., L. R. Natkin, R. M. Fujita, Y. Wei, H. A. Chapman (1997): Plasmin and plasminogen activator inhibitor type 1 promote cellular motility by regulating the interaction between the urokinase receptor and vitronectin. J. Clin. Invest. 100, 58-67.
61. Yamashita, H., H. Ichijo, S. Grimsby, A. Morén, P. ten Dijke, K. Miyazono (1994): Endoglin forms a heteromeric complex with the signaling receptors for transforming growth factor β. J. Biol. Chem. 269, 1995-2001.
62. Zhang, H., A. Mak, A. R. E. Shaw, M. Letarte (1996): Endoglin is a component of the functional TGF-β receptor complex of human pre-B leukemic cells. J. Immunol. 156, 565-573.