Thrombospondin-1 induces tyrosine phosphorylation of adherens junction proteins and regulates an endothelial paracellular pathway

Molecular Biology of the Cell

Volumn 10, Issue 5, 1999, Pages 1537-1551

  Goldblum, Simeon E ^a   Young, Bradford A ^a   Wang, Ping ^a   Murphy Ullrich, Joanne E ^b  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA TUBULIN; BOVINE SERUM ALBUMIN; CARBON 14; COLLAGEN TYPE 1; FIBRONECTIN; GENISTEIN; HERBIMYCIN A; PHOSPHOTYROSINE; PROTEIN TYROSINE KINASE; THROMBOSPONDIN 1; TRANSFORMING GROWTH FACTOR BETA; VITRONECTIN;

ANIMAL CELL; ARTICLE; CATTLE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME INHIBITION; LUNG ARTERY; MONOLAYER CULTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ANIMALIA; BOS TAURUS; BOVINAE;

EID: 0032896852     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.10.5.1537     Document Type: Article

References (65)

1. Abedi, H., and Zachary, I. (1997). Vascular endothelial growth factor stimulates tyrosine phosphorylation and recruitment to new focal adhesions of focal adhesion kinase and paxillin in endothelial cells. J. Biol. Chem. 272, 15442-15451.
2. Adams, J.C. (1995). Formation of stable microspikes containing actin and the 55 kDa actin bundling protein, fascin, is a consequence of cell adhesion to thrombospondin-1: implications for the antiadhesive activities of thrombospondin-1. J. Cell Sci. 108, 1977-1990.
3. Alessio, M., DeMonte, L., Scirea, A., Gruarin, P., Tandon, N.N., and Sitia, R. (1996). Synthesis, processing and intracellular transport of CD36 during monocytic differentiation. J. Biol. Chem. 271, 1770-1776.
4. Balsamo, J., Ernst, H., Zanin, M.K.B., Hoffman, S., and Lilien, J. (1995). The interaction of the retina cell surface N-acetylgalactosaminylphosphotransferase with an endogenous proteoglycan ligand results in inhibition of cadherin-mediated adhesion. J. Cell Biol. 129, 1391-1401.
5. Barth, A.I.M., Nathke, I.S., and. Nelson, W.J. (1997). Cadherins, catenins and APC protein: interplay between cytoskeletal complexes and signaling pathways. Curr. Opin. Cell Biol. 9, 683-690.
6. Behrens, J., Vakaet, L., Friis, R., Winterhager, E., Roy, F.V., Mareel, M.M., and Birchmeier, W. (1993). Loss of epithelial differentiation and gain of invasiveness correlates with tyrosine phosphorylation of the E-cadherin/β-catenin complex in cells transformed with a temperature-sensitive v-src gene. J. Cell Biol. 120, 757-766.
7. v integrin cytoplasmic tail. J. Biol. Chem. 271, 31458-31462.
8. Bornstein, P. (1995). Diversity of function is inherent in matricellular proteins: an appraisal of thrombospondin 1. J. Cell Biol. 130, 503-506.
9. Botney, M.D., Kaiser, L.R., Cooper, J.D., Mecham, R.P., Parghi, D., Rody, J., and Parks, W.C. (1992). Extracellular matrix protein gene expression in atherosclerotic hypertensive pulmonary arteries. Am. J. Pathol. 140, 357-364.
10. Brady-Kalnay, S.M., Rimm, D.L., and Tonks, N.K. (1995). Receptor protein tyrosine phosphatase PTPμ associates with cadherins and catenins in vivo. J. Cell Biol. 130, 977-986.
11. Bull, H.A., Brickell, P.M., and Dowd, P.M. (1994). Src-related protein tyrosine kinases are physically associated with the surface antigen CD36 in human dermal microvascular endothelial cells. FEBS Lett. 352, 41-44.
12. FAK accompanies cell adhesion to extracellular matrix: a role in cytoskeletal assembly. J. Cell Biol. 119, 893-903.
13. Bussolino, F., Camussi, G., Aglietta, M., Braquet, P., Bosia, A., Pescarmona, G., Sanavio, F., D'Urso, N., and Marchisio, P.C. (1987). Human endothelial cells are target for platelet-activating factor. I. Platelet-activating factor induces changes in cytoskeleton structures. J. Immunol. 139, 2439-2446.
14. Chrzanowska-Wodnicka, M., and Burridge, K. (1996). Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133, 1403-1415.
15. Clark, E.A., and Brugge, J.S. (1995). Integrins and signal transduction pathways: the road taken. Science 268, 233-238.
16. Crawford, S.E., Stellmach, V., Murphy-Ullrich, J.E., Ribeiro, S.M.F., Lawler, J., Hynes, R.O., Boivin, G.P., and Bouck, N. (1998). Thrombospondin-1 is a major activator of TGF-β1 in vivo. Cell 93, 1159-1170.
17. DiPietro, L.A., Nissen, N.N., Gamelli, R.L., Koch, A.E., Pyle, J.M., and Polverini, P.J. (1996). Thrombospondin 1 synthesis and function in wound repair. Am. J. Pathol. 148, 1851-1860.
18. Esser, S., Lampugnani, M.G., Corada, M., Dejana, E., and Risau, W. (1998). Vascular endothelial growth factor induces VE-cadherin tyrosine phosphorylation in endothelial cells. J. Cell Sci. 111, 1853-1865.
19. Fuchs, M., Muller, T., Lerch, M.M., and Ullrich, A. (1996). Association of the human protein-tyrosine phosphatase K with members of the armadillo family. J. Biol. Chem. 271, 16712-16719.
20. Gaits, F., Li, R.Y., Ragab, A., Ragab-Thomas, J.M.F., and Chap, H. (1995). Increase in receptor-like protein tyrosine phosphatase activity and expression level on density-dependent growth arrest of endothelial cells. Biochem. J. 311, 97-103.
21. Gao, A.G., Lindberg, F.P., Dimitry, J.M., Brown, E.J., and Frazier, W.A. (1996). Thrombospondin modulates alpha v beta 3 function through integrin-associated proteins. J. Cell Biol. 135, 533-544.
22. Goldblum, S.E., Brann, T.W., Ding, X., Pugin, J., and Tobias, P.S. (1994). Lipopolysaccharide (LPS)-binding protein and soluble CD14 function as accessory molecules for LPS-induced changes in endothelial barrier function in vitro. J. Clin. Invest. 93, 692-702.
23. Goldblum, S.E., Ding, X., Brann, T.W., and Campbell-Washington, J. (1993). Bacterial lipopolysaccharide induces actin reorganization, intercellular gap formation, and endothelial barrier dysfunction in pulmonary vascular endothelial cells: concurrent F-actin depolymerization and new actin synthesis. J. Cell. Physiol. 157, 13-23.
24. Goldblum, S.E., Ding, X., Funk, S.E., and Sage, E.H. (1994a). SPARC (secreted protein acidic and rich in cysteine) regulates endothelial cell shape and barrier function. Proc. Natl. Acad. Sci. USA 91, 3448-3452.
25. Greenwalt, D.E, and Mather, I.H. (1985). Characterization of an apically derived epithelial membrane glycoprotein from bovine milk, which is expressed in capillary endothelia in diverse tissues. J. Cell Biol. 100, 397-408.
26. Gumbiner, B.M. (1996). Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84, 345-357.
27. v-src causes tyrosine phosphorylation and inactivation of the N-cadherin-catenin cell adhesion system. EMBO J. 12, 307-314.
28. Hazan, R.B., and Norton, L. (1998). The epidermal growth factor receptor modulates the interaction of E-cadherin with the actin cytoskeleton. J. Biol. Chem. 273, 9078-9084.
29. Hoschuetzky, H., Aberle, H., and Kemler, R. (1994). β-catenin mediates the interaction of the cadherin-catenin complex with epidermal growth factor receptor. J. Cell Biol. 127, 1375-1380.
30. Incardona, F., Lewalle, J.M., Morandi, V., Lambert, S., Legrand, Y., Foidart, J.M., and Legrand, C. (1995). Thrombospondin modulates human breast adenocarcinoma cell adhesion to human endothelial cells. Cancer Res. 55, 166-173.
31. Iruela-Arispe, M.L., Bornstein, P., and Sage, H. (1991). Thrombospondin exerts an antiangiogenic effect on cord formation by endothelial cells in vitro. Proc. Natl. Acad. Sci. USA 88, 5026-5030.
32. Kemler, R. (1993). From cadherins to catenins: cytoplasmic protein interactions and regulation of cell adhesion. Trends Genet. 9, 317-321.
33. Kuhn, C., and Mason, R.J. (1995). Immunolocalization of SPARC, tenascin, and thrombospondin in pulmonary fibrosis. Am. J. Pathol. 147, 1759-1769.
34. Lahav, J. (1993). The functions of thrombospondin and its involvement in physiology and pathophysiology. Biochim. Biophys. Acta 1182, 1-14.
35. Lampugnani, M.G., Corada, M., Andriopoulou, P., Esser, S., Risau, W., and Dejana, E. (1997). Cell confluence regulates tyrosine phosphorylation of adherens junction components in endothelial cells. J. Cell Sci. 110, 2065-2077.
36. Lampugnani, M.G., Corada, M., Caveda, L., Breviario, F., Ayalon, O., Geiger, B., and Dejana, E. (1995). The molecular organization of endothelial cell to cell junctions: differential association of plakoglobin, β-catenin, and a-catenin with vascular endothelial cadherin (VE-cadherin). J. Cell Biol. 129, 203-217.
37. Lawler, J., Weinstein, R., and Hynes, R.O. (1988). Cell attachment to thrombospondin: the role of ARG-GLY-ASP, calcium, and integrin receptors. J. Cell Biol. 107, 2351-2361.
38. FAK and paxillin are substrates for bradykinin-stimulated tyrosine phosphorylation in swiss 3T3 cells. J. Biol. Chem. 269, 24328-24334.
39. Luscinskas, F.W., Cybulsky, M.I., Kiely, J.M., Peckins, C.S., Davis, V.M., and Gimbrone, M.A., Jr. (1991). Cytokine-activated human endothelial monolayers support enhanced neutrophil transmigration via a mechanism involving both endothelial-leukocyte adhesion molecule-1 and intercellular adhesion molecule-1. J. Immunol. 146, 1617-1625.
40. Malik, A.B., Lynch, J.J., and Cooper, J.A. (1989). Endothelial barrier function. J. Invest. Dermatol. 93, 62S-67S.
41. Mansfield, P.J., Boxer, L.A., and Suchard, S.J. (1990). Thrombospondin stimulates motility of human neutrophils. J. Cell Biol. 111, 3077-3086.
42. Matsuyoshi, N., Hamaguchi, M., Taniguchi, S., Nagafuchi, A., Tsukita, S., and Takeichi, M. (1992). Cadherin-mediated cell-cell adhesion is perturbed by v-src tyrosine phosphorylation in metastatic fibroblasts. J. Cell Biol. 118, 703-714.
43. Mosher, D.F. (1990). Physiology of thrombospondin. Annu. Rev. Med. 41, 85-97.
44. Munjal, I.D., Blake, D.A., Sabet, M.D., and Gordon, S.R. (1990). Thrombospondin: biosynthesis, distribution, and changes associated with wound repair in corneal endothelium. Eur. J. Cell Biol. 52, 252-263.
45. Murphy-Ullrich, J.E. (1995). Antiadhesive proteins of the extracellular matrix: thrombospondin, tenascin, and SPARC. Trends Glycosci. Glycotechnol. 7, 89-100.
46. Murphy-Ullrich, J.E., Schultz-Cherry, S., and Höök, M. (1992). Transforming growth factor-β complexes with thrombospondin. Mol. Biol. Cell 3, 181-188.
47. O'Shea, K.S., and Dixit, V.M. (1988). Unique distribution of the extracellular matrix component thrombospondin in the developing mouse embryo. J. Cell Biol. 107, 2737-2748.
48. O'Shea, K.S., Rheinheimer, J.S.T., and Dixit, V.M. (1990). Deposition and role of thrombospondin in the histogenesis of the cerebellar cortex. J. Cell Biol. 110, 1275-1283.
49. Parsons, J.T., and Parsons, S.J. (1997). Src family ryrosine kinases: cooperating with growth factor and adhesion signaling pathways. Curr. Opin. Cell Biol. 9, 187-192.
50. Roberts, A., and Sporn, M.B. (1993). Physiological actions and clinical applications of transforming growth factor-β (TGF-β). Growth Factors 8, 1-9.
51. Roberts, D.D. (1996). Regulation of tumor growth and metastasis by thrombospondin-1. FASEB J. 10, 1183-1191.
52. Sage, E.H., and Bornstein, P. (1991). Extracellular proteins that modulate cell-matrix interactions. J. Biol. Chem. 266, 14831-14834.
53. Schaphorst, K.L., Pavalko, F.M., Patterson, C.E., and Garcia, J.G. (1997). Thrombin-mediated focal adhesion plaque reorganization in endothelium: role of protein phosphorylation. Am. J. Respir. Cell Mol. Biol. 17, 443-455.
54. Schultz-Cherry, S., and Murphy-Ullrich, J.E. (1993). Thrombospondin causes activation of latent transforming growth factor-β secreted by endothelial cells by a novel mechanism. J. Cell Biol. 122, 923-932.
55. Schultz-Cherry, S., Chen, H., Mosher, D.F., Misenheimer, T.M., Krutzsch, H.C., Roberts, D.D., and Murphy-Ullrich, J.E. (1995). Regulation of transforming growth factor-β activation by discrete sequences of thrombospondin 1. J. Biol. Chem. 270, 7304-7310.
56. Shasby, D.M., Shasby, S.S., Sullivan, J.M., and Peach, M.J. (1982). Role of endothelial cell cytoskeleton in control of endothelial permeability. Circ. Res. 51, 657-661.
57. Shibamoto, S., Hayakawa, M., Takeuchi, K., Hori, T., Oku, N., Miyazawa, K., Kitamura, M., Takeichi, N., and Ito, F. (1994). Tyrosine phosphorylation of β-catenin and plakoglobin enhanced by hepatocyte growth factor and the epidermal growth factor in human carcinoma cells. Cell Adhes. Commun. 1, 295-305.
58. FAK) in human endothelial cells. Oncogene 13, 515-525.
59. Southey, M.C., Findlay, D.M., and Kemp, B.E. (1995). Regulation of membrane-associated tyrosine phosphatases in UMR 106.06 osteoblast-like cells. Biochem. J. 305, 485-490.
60. Taraboletti, G., Roberts, D.D., and Liotta, L.A. (1987). Thrombospondin-induced tumor cell migration: haptotaxis and chemotaxis are mediated by different molecular domains. J. Cell Biol. 105, 2409-2415.
61. Taraboletti, G., Roberts, D., Liotta, L.A., and Giavazzi, R. (1990). Platelet thrombospondin modulates endothelial cell adhesion, motility, and growth: a potential angiogenesis regulatory factor. J. Cell Biol. 111, 765-772.
62. Tsukita, S., Oishi, K., Akiyama, T., Yamanashi, Y., Yamamoto, T., and Tsukita, S. (1991). Specific proto-oncogenic tyrosine kinases of src family are enriched in cell-to-cell adherens junctions where the level of tyrosine phosphorylation is elevated. J. Cell Biol. 113, 867-879.
63. Volberg, T., Zick, Y., Dror, R., Sabanay, I., Gilon, C., Levitzki, A., and Geiger, B. (1992). The effect of tyrosine-specific protein phosphorylation on the assembly of adherens-type junctions. EMBO J. 11, 1733-1742.
64. Wong, M.K.K., and Gotlieb, A.I. (1986). Endothelial cell monolayer integrity. I. Characterization of dense peripheral band of microfilaments. Arteriosclerosis 6, 212-219.
65. Young, B.A., Wang, P., and Goldblum, S.E. (1998). The counteradhesive protein SPARC regulates an endothelial paracellular pathway protein tyrosine. Biochem. Biophys. Res. Commun. 251, 320-327.