PECAM-1 (CD31) functions as a reservoir for and a modulator of tyrosine-phosphorylated β-catenin

Journal of Cell Science

Volumn 112, Issue 18, 1999, Pages 3005-3014

  Ilan, Neta ^a   Mahooti, Sepi ^a   Rimm, David L ^a   Madri, Joseph A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

catenin; PECAM 1 CD31; Tyrosine phosphorylation; VEGF

Indexed keywords

BETA CATENIN; CD31 ANTIGEN; VASCULOTROPIN; VASCULOTROPIN RECEPTOR;

ARTICLE; CARCINOMA CELL; CELL CONTACT; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ANIMALS; ANTIGENS, CD31; BETA CATENIN; CATTLE; CELLS, CULTURED; CYTOSKELETAL PROTEINS; ENDOTHELIAL GROWTH FACTORS; ENDOTHELIUM, VASCULAR; GENE EXPRESSION; HUMANS; LYMPHOKINES; MODELS, BIOLOGICAL; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; TRANS-ACTIVATORS; TRANSFECTION; TYROSINE; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTORS;

EID: 0032877293     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     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 local adhesion kinase and paxillin in endothelial cells. J. Biol. Chem. 272, 15442-15451
2. Alon, T., Hemo, I., Itin, A., Peer, J., Stone, J. and Keshet, E. (1995). Vascular endothelial growth factor acts as a survival factor for newly formed retinal vessels and has implications for retinopathy of prematurity. Nature Med. 1, 1024-1028.
3. Ayalon, O., Sabani, H., Lampugnani, M-G., Dejana, E. and Geiger, B. (1994). Spatial and temporal relationship between cadherin and PECAM-1 in cell-cell junctions of human endothelial cells. J. Cell Biol. 126, 247-258.
4. Balsamo, J., Leung, T. C., Ernst, H., Zanin, M. K. B., Hoffman, S. and Lilien, J. (1996). Regulated binding of a PTP1B-like phosphatase to N-cadherin: Control of cadherin-mediated adhesion by dephosphorylation of β-catenin. J. Cell Biol. 134, 801-813.
5. Balsamo, J., Arregui, C., Leung, T. C. and Lilien, J. (1998). The nonreceptor protein tyrosine phosphatase PTP1B binds to the cytoplasmic domain of N-cadherin and regulates the cadherin-actin linkage. J. Cell Biol. 143, 523-532.
6. 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.
7. Beck, L. and D'Amore, P. A. (1997). Vascular development: cellular and molecular regulation. FASEB J. 11, 365-373.
8. Behrens, J., Vakaet, L., Frriis, R., Winterhager, E., Van Roy, F., 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.
9. Benjamin, L. E. and Keshet, E. (1997). Conditional switching of vascular endothelial growth factor (VEGF) expression in tumors: Induction of endothelial cell shedding and regression of hemangioblastoma-like vessels by VEGF withdrawal. Proc. Nat. Acad. Sci. USA 94. 8761-8766.
10. Ben-Ze'ev, A. and Geiger, B. (1998). Differential molecular interactions of β-catenin and plakoglobin in adhesion, signaling and cancer. Curr. Opin. Cell Biol. 10, 629-639.
11. Birchmeier, C., Birchmeier, W. and Brand-Saberi, B. (1996). Epithelial-mesenchymal transition in cancer progression. Acta Anat. 156, 217-226.
12. Bogen, S., Pak, J., Garifallou, M., Deng, X. and Muller, W. A. (1994). Monoclonal antibody to murine PECAM-1 (CD31) block acute inflammation in vivo. J. Exp. Med. 179, 1059-1064.
13. Brown, J. D. and Moon, R. T. (1998). Wnt signaling: why is everything so negative? Curr. Opin. Cell Biol. 10. 182-187.
14. Cao, M. Y., Huber, M., Beauchemin, N., Famiglietti, J., Albelda, S. M. and Veillette, A. (1998). Regulation of mouse PECAM-1 tyrosine phosphorylation by the Src and Csk families of protein-tyrosine kinases. J. Biol. Chem. 273, 15765-15772.
15. Conn, G., Bayne, M., Soderman, L., Kwok, P. W., Sullivan, K. A., Palisi, T. M., Hope, D. A. and Thomas, K. A. (1990). Amino acid and cDNA sequence of a vascular endothelial cell mitogen homologous to platelet-derived growth factor. Proc. Nat. Acad. Sci. USA 87, 2628-2632.
16. Connolly, D. T., Olander, J. V., Heuvelman, D., Nelson, R., Monsell, R., Siegel, N., Haymore, B. L., Leimgruber, R. and Feder, J. (1989). Human vascular permeability factor. Isolation from U937 cells. J. Biol. Chem. 254, 20017-20024.
17. Daniel, J. M. and Reynolds, A. B. (1997). Tyrosine phosphorylation and cadherin/catenin function. BioEssays 19, 883-891.
18. DeLisser, H. M., Newman, P. J. and Albelda, S. M. (1994). Molecular and functional aspects of PECAM-1/CD31. Immunol. Today 15, 490-495.
19. DeLisser, H. M., Christofidou-Solomidou, M., Strier, R. M., Burdick, M. D., Robinson, C. S., Wexler, R. S., Kerr, J. S., Garland, C., Merwin, J. R., Madri, J. A. and Albelda, S. M. (1997). Involvement of endothelial PECAM-1/CD31 in angiogenesis. Am. J. Pathol. 151, 671-677.
20. Dillon, D. A., Daquila, T., Reynolds, A. B., Fearon, E. R. and Rimm, D. L. (1998). The expression of P120ctn protein In breast cancer is independent of alpha- and beta-catenin and E-cadherin. Am. J. Pathol. 152. 75-82.
21. 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.
22. Ferrara, N. and Davis-Smyth, T. (1997). The biology of vascular endothelial growth factor. Endocr. Rev. 18, 4-25.
23. Folkman, J. and D'Amore, P. A. (1996). Blood vessel formation: What is its molecular basis. Cell 87, 1153-1155.
24. Gilbert, R. E., Vranes, D., Berka, J. L., Kelly, D. J., Cox, A., Wu, L. L., Stacter, S. A. and Cooper, M. E. (1998). Vascular endothelial growth factor and its receptors in control and diabetic rat eyes. Lab. Invest. 78, 1017-1027.
25. Hanahan, D. and Folkman, J. (1996). Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86, 353-364.
26. Hanahan, D. (1997). Signaling vascular morphogenesis and maintenance. Science 277, 48-50.
27. 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.
28. Ikeda, S., Kishida, S., Yamamoto, H., Murai, H., Koyama, S. and Kikuchi, A. (1998). Axin, a negative regulator of the Wnt signaling pathway, forms a complex with Gsk-3-beta and beta-catenin and promotes Gsk-3-beta-dependent phosphorylation of beta-catenin. EMBO J. 17, 1371-1384.
29. Ilan N., Mahooti, S. and Madri, J. A. (1998). Distinct signal transduction pathways are utilized during the tube formation and survival phases of in vitro angiogenesis. J. Cell Sci. 111, 3621-3631.
30. Jackson, D. E., Kupcho, K. R. and Newman, P. J. (1997a). Characterization of phosphotyrosine binding motifs in the cytoplasmic domain of platelet/endothelial cell adhesion molecule-1 (PECAM-1) that are required for the cellular association and activation of the protein-tyrosine phosphatase. SHP-2. J. Biol. Chem. 272, 24868-24875.
31. Jackson, D. E., Ward, C. M., Wang, R. and Newman, P. J. (1997b). The protein-tyrosine phosphatase SHP-2 binds platelet/endothelial cell adhesion molecule-1 (PECAM-1) and forms a distinct signaling complex during platelet aggregation. J. Biol. Chem. 272, 6986-6993.
32. Jakeman, L. B., Winer, J., Bennett, G. L., Altar, C. A. and Ferrara, N. (1992). Binding sites for vascular endothelial growth factor are localized on endothelial cells in adult rat tissues. J. Clin. Invest. 89, 244-253.
33. Jakeman L. B., Armanini, M., Phillips, H. S. and Ferrara, N. (1993). Developmental expression of binding sites and mRNA for vascular endothelial growth factor suggests a role for this protein in vasculogenesis and angiogenesis. Endocrinology 133, 848-859.
34. Keck, P. J., Hauser, S. D., Krivi, G., Sanzo, K., Warren, T., Feder, J. and Connolly, D. T. (1989). Vascular permeability factor, an endothelial cell mitogen related to platelet derived growth factor. Science 246, 1309-1312.
35. Kevil, C. G., Payne, D. K., Mire, E. and Alexander, J. S. (1998) Vascular permeability factor/ vascular endothelial cell growth factor-mediated permeability occurs through disorganization of endothelial junctional proteins. J. Biol. Chem. 273, 15099-15103.
36. Kim, C. S., Wang, T. and Madri, J. A. (1998). Platelet endothelial cell adhesion molecule-1 expression modulates endothelial cell migration in vitro. Lab. Invest. 78, 583-590.
37. Kinch, M. S., Clark, G. J., Der, C. J. and Burridge, K. (1995). Tyrosine phosphorylation regulates the adhesion of ras-transformed breast epithelia. J. Cell Biol. 130, 461-471.
38. Koslov, E. R., Maupin, P., Pradhan, D., Morrow, J. S. and Rimm, D. L. (1997). Alpha-catenin can form asymmetric homodimeric complexes and/or heterodimeric complexes with beta-catenin. J. Biol. Chem. 272, 27301-27306.
39. Kubota, Y., Kleinman, H. K., Martin, G. R. and Lawley, T. J. (1988). Role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures. J. Cell Biol. 107, 1589-1598.
40. Leung, D. W., Cachianes, G., Kuang, W.-J., Doeddel, D. V. and Ferrara, N. (1989). Vascular endothelial growth factor is a secreted angiogenic mitogen. Science 246, 1306-1309.
41. Lu, T. T., Yan, L. G. and Madri, J. A. (1996). Integrin engagement mediates tyrosine dephosphorylation on platelet-endothelial cell adhesion molecule 1. Proc. Nat. Acad. Sci. USA 93, 11808-11813.
42. Lu, T. T., Barreuther, M., Davis, S. and Madri, J. A. (1997). Platelet endothelial cell adhesion molecule-1 is phosphorylatable by c-Src, binds Src-Src homolgy 2 domain, and exhibits immunoreceptor tyrosine-based activation motif-like properties. J. Biol. Chem. 272, 14442-14446.
43. Matsumura, T., Wolff, K. and Petzelbauer, P. (1997). Endothelial cell tube formation depends on cadherin 5 and CD31 interactions with filamentous actin. J. Immunol. 158, 3408-3416.
44. Muller, W. A., Weigel, S. A., Deng, X. and Phillips, D. M. (1993) PECAM-1 is required for transendothelial migration of leukocytes. J. Exp. Med. 178, 449-460.
45. Newman, P. J. (1997). The biology of PECAM-1. J. Clin. Invest. 99, 3-8.
46. Newman, P. J. (1999). Switched at birth: a new family for PECAM-1. J. Clin. Invest. 103, 5-9
47. Norton, A., Jordan, S. and Yeomans, P. (1994). Brief high-temperature heat denaturation (pressure cooking): a simple and effective method of antigen retrieval for routinely processed specimens. J. Pathol. 173, 371-379.
48. Obeso, J., Weber, J. and Auerbach, R. (1990). A hemangioendothelioma-derived cell line: Its use as a model for the study of endothelial cell biology. Lab. Invest. 63, 259-269.
49. Pinter, E., Barreuther, M., Lu, T., Imhof, B. A. and Madri, J. A. (1997). Platelet-endothelial cell adhesion molecule-1 (PECAM-1/CD31) tyrosine phosphorylation state changes during vasculogenesis in the murine conceptus. Am. J. Pathol. 150, 1523-1530.
50. Pinter, E., Mahooti, S., Wang, Y., Imhof, B. A. and Madri, J. A. (1999). Hyperglycemia-induced vasculopathy in the murine vitelline vasculature: correlation with PECAM-1/CD31 tyrosine phosphorylation state. Am. J. Pathol. 154, 1367-1379.
51. Plouet J., Schilling, J. and Gospodarowicz, D. (1989). Isolation and characterization of a newly identified endothelial cell mitogen produced by AtT20 cells. EMBO J. 8, 3801-3806.
52. Risau, W. (1997). Mechanisms of angiogenesis. Nature 386, 671-674.
53. Rubinfeld, B., Souza, B., Albert, I., Muller, O., Chamberlain, S. H., Masiarz, F. R., Munemitsu, S. and Polakis, P. (1993). Association of the APC gene product with beta-catenin. Science 262, 1734-1737.
54. Sage, E. H. (1997). Pieces of eight: bioactive fragments of extracellular proteins as regulators of angiogenesis. Trends Cell Biol. 7, 182-186.
55. Salomon, D., Ayalon, O., Patel-King, R., Hynes, R. and Geiger, B. (1992). Extrajunctional distribution of N-cadherin in cultured human endothelial cells. J. Cell Sci. 102, 7-17.
56. Sakanaka, C., Weiss, J. B. and Williams, L. T. (1998). Bridging of beta-catenin and glycogen synthase kinase-3-beta by axin and inhibition of beta-catenin-mediated transcription. Proc. Nat. Acad. Sci. USA 95, 3020-3023.
57. Senger, D. R., Galli, S. J., Dvorak, A. M., Perruzzi, C. A., Harvey, V. S. and Devorak, H. F. (1983). Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219, 983-985.
58. Shibamoto, S., Hayakawa, M., Takeuchi, K., Hori, T., Oku, N., Miyazawa, K., Kitamura, N., Takeichi, M. and Ito, F. (1994). Tyrosine phosphorylation of beta-catenin and plakoglobin enhanced by hepatocyte growth factor and epidermal growth factor in human carcinoma cells. Cell Adhes. Commun. 1, 295-305.
59. Simcha I., Shtutman, M., Salomon, D., Zhurinsky, J., Sadot, E., Geiger, B. and Ben-Ze'ev, A. (1998). Differential nuclear translocation and transactivalion potential of β-catenin and plakoglobin. J. Cell Biol. 141, 1433-1448.
60. Sommers, C. L., Gelmann, E. P., Kemler, R., Cowin, P. and Byers, S. W. (1994). Alterations in beta-catenin phosphorylation and plakoglobin expression in human breast cancer cells. Cancer Res. 54, 3544-52.
61. Stromblad, S. and Cheresh, D. A. (1996). Cell adhesion and angiogenesis. Trends Cell Biol. 6, 462-468.
62. Takahashi, K., Mulliken, J. B., Kozakewich, H. P. W., Rogers, R. A., Folkman, J. and Ezekowitz, A. B. (1994). Cellular markers that distinguish the phases of hemangioma during infancy and childhood. J. Clin. Invest. 93, 2357-2364.
63. Vaporciyan, A. A., DeLisser, H. M., Yan, H., Mendiguren, I. I., Thom, S. R., Jones, M. L., Ward, P. A. and Albelda, S. M. (1993). Involvement of platelet endothelial cell adhesion molecule-1 in neutrophil recruitment in vivo. Science 262, 1580-1582.
64. Vermeulen S. J., Bruyneel, E. A., Bracke, M. E., De Bruyne, G. K., Vennekens, K. M., Vleminckx, K. L., Berx, G. J., van Roy, F. M. and Mareel, M. M. (1995). Transition from the noninvasive to the invasive phenotype and loss of α-catenin in human colon cancer cells. Cancer Res. 55, 4722-4728.
65. Whitehead, I., Kirk, H. and Kay, R. (1995). Expression cloning of oncogenes by retroviral transfer of cDNA libraries. Mol. Cell. Biol. 15, 704-710.