Angiopoietin-1-induced ubiquitylatIon of Tie2 by c-Cbl is required for internalization and degradation

Biochemical Journal

Volumn 423, Issue 3, 2009, Pages 375-380

  Wehrle, Christina ^a,b   Van Slyke, Paul ^a   Dumont, Daniel J ^a,b  

^a Sunnybrook Health Sciences Centre   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Angiogenesis; Receptor trafficking; Receptor tyrosine kinase; Tie2; Ubiquitin

Indexed keywords

ANGIOGENESIS; RECEPTOR TRAFFICKING; RECEPTOR TYROSINE KINASE; TIE2; UBIQUITIN;

AMINO ACIDS; BIOACTIVITY; DEGRADATION; LIGANDS; MACHINERY; PROTEINS;

ENDOTHELIAL CELLS;

ANGIOPOIETIN 1; ANGIOPOIETIN RECEPTOR; CBL PROTEIN;

ANGIOGENESIS; ARTICLE; CONTROLLED STUDY; GENE DELETION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INTERNALIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; UBIQUITINATION; VASCULAR RESISTANCE;

ANGIOPOIETIN-1; CELL LINE; HUMANS; ONCOGENE PROTEIN V-CBL; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-CBL; RECEPTOR, TIE-2; SIGNAL TRANSDUCTION; UBIQUITINATION;

MUS;

EID: 70350101449     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20091010     Document Type: Article

References (39)

1. Partanen, J., Armstrong, E., Makela, T. P., Korhonen, J., Sandberg, M., Renkonen, R., Knuutila, S., Huebner, K. and Alitalo, K. (1992) A novel endothelial cell surface receptor tyrosine kinase with extracellular epidermal growth factor homology domains. Mol. Cell. Biol. 12, 1698-1707
2. Dumont, D. J., Yamaguchi, T. P., Conlon, R. A., Rossant, J. and Breitman, M. L. (1992) tek, a novel tyrosine kinase gene located on mouse chromosome 4, is expressed in endothelial cells and their presumptive precursors. Oncogene 7, 1471-1480
3. Iwama, A., Hamaguchi, I., Hashiyama, M., Murayama, Y., Yasunaga, K. and Suda, T. (1993) Molecular cloning and characterization of mouse TIE and TEK receptor tyrosine kinase genes and their expression in hematopoietic stem cells. Biochem. Biophys. Res. Commun. 195, 301-309
4. Korhonen, J., Partanen, J., Armstrong, E., Vaahtokari, A., Elenius, K., Jalkanen, M. and Alitalo, K. (1992) Blood. 80, 2548-2555
5. Dumont, D. J., Gradwohl, G., Fong, G. H., Puri, M. C., Gertsenstein, M., Auerbach, A. and Breitman, M. L. (1994) Genes. Dev. 8, 1897-1909
6. Thurston, G., Rudge, J. S., Ioffe, E., Zhou, H., Ross, L., Croll, S. D., Glazer, N., Holash, J., McDonald, D. M. and Yancopoulos, G. D. (2000) Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat. Med. 6, 460-463
7. Gamble, J. R., Drew, J., Trezise, L., Underwood, A., Parsons, M., Kasminkas, L., Rudge, J., Yancopoulos, G. and Vadas, M. A. (2000) Angiopoietin-1 is an antipermeability and anti-inflammatory agent in vitro and targets cell junctions. Circ. Res. 87, 603-607
8. Hayes, A. J., Huang, W. Q., Mallah, J., Yang, D., Lippman, M. E. and Li, L. Y. (1999) Angiopoietin-1 and its receptor Tie-2 participate in the regulation of capillary-like tubule formation and survival of endothelial cells. Microvasc. Res. 58, 224-237
9. Koblizek, T. I., Weiss, C., Yancopoulos, G. D., Deutsch, U. and Risau, W. (1998) Angiopoietin-1 induces sprouting angiogenesis in vitro. Curr. Biol. 8, 529-532
10. Kim, I., Kim, H. G., Moon, S. O., Chae, S. W., So, J. N., Koh, K. N., Ahn, B. C. and Koh, G. Y. (2001) Angiopoietin-1 induces endothelial cell sprouting through the activation of focal adhesion kinase and plasmin secretion. Circ. Res. 86, 952-999
11. Master, Z., Jones, N., Tran, J., Jones, J., Kerbel, R. S. and Dumont, D. J. (2001) Dok-R plays a pivotal role in angiopoietin-1-dependent cell migration through recruitment and activation of Pak. EMBO J. 20, 5919-5928
12. Witzenbichler, B., Maisonpierre, P. C., Jones, P., Yancopoulos, G. D. and Isner, J. M. (1998) Chemotactic properties of angiopoietin-1 and -2, ligands for the endothelial-specific receptor tyrosine kinase Tie2. J. Biol. Chem. 273, 18514-18521
13. Kontos, C. D., Stauffer, T. P., Yang, W. P., York, J. D., Huang, L., Blanar, M. A., Meyer, T. and Peters, K. G. (1998) Tyrosine 1101 of Tie2 is the major site of association of p85 and is required for activation of phosphatidylinositol 3-kinase and Akt. Mol. Cell Biol. 18, 4131-4140
14. Kim, I., Kim, H. G., So, J. N., Kim, J. H., Kwak, H. J. and Koh, G. Y. (2000) Angiopoietin-1 regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Circ. Res. 86, 24-29
15. Davis, S., Aldrich, T. H., Jones, P. F., Acheson, A., Compton, D. L., Jain, V., Ryan, T. E., Bruno, J., Radziejewski, C., Maisonpierre, P. C. and Yancopoulos, G. D. (1996) Isolation of angiopoietin-1, a ligand for the TIE2 receptor, by secretion-trap expression cloning. Cell 87, 1161-1169
16. Xu, Y. and Yu, Q. (2001) Angiopoietin-1, unlike angiopoietin-2, is incorporated into the extracellular matrix via its linker peptide region. J. Biol. Chem. 276, 34990-34998
17. Suri, C., Jones, P. F., Patan, S., Bartunkova, S., Maisonpierre, P. C., Davis, S., Sato, T. N. and Yancopoulos, G. D. (1996) Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell 87, 1171-1180
18. Hashimoto, T., Wu, Y., Boudreau, N., Li, J., Matsumoto, M. and Young, W. (2004) Regulation of tie2 expression by angiopoietin-potential feedback system. Endothelium 11, 207-210
19. Bogdanovic, E., Nguyen, V. P. and Dumont, D. J. (2006) Activation of Tie2 by angiopoietin-1 and angiopoietin-2 results in their release and receptor internalization. J. Cell Sci. 119, 3551-3560
20. Saharinen, P., Eklund, L., Miettinen, J., Wirkkala, R., Anisimov, A., Winderlich, M., Nottebaum, A., Vestweber, D., Deutsch, U., Koh, G. Y. et al. (2008) Angiopoietins assemble distinct Tie2 signalling complexes in endothelial cell-cell and cell-matrix contacts. Nat. Cell Biol. 10, 527-537
21. Fukuhara, S., Sako, K., Minami, T., Noda, K., Kim, H. Z., Kodama, T., Shibuya, M., Takakura, N., Koh, G. Y. and Mochizuki, N. (2008) Differential function of Tie2 at cell-cell contacts and cell-substratum contacts regulated by angiopoietin-1. Nat. Cell Biol. 10, 513-526
22. de Melker, A. A., van der, H. G., Calafat, J., Jansen, H. and Borst, J. (2001) c-Cbl ubiquitinates the EGF receptor at the plasma membrane and remains receptor associated throughout the endocytic route. J. Cell Sci. 114, 2167-2178
23. Schlesinger, D. H., Goldstein, G. and Niall, H. D. (1975) The complete amino acid sequence of ubiquitin, an adenylate cyclase stimulating polypeptide probably universal in living cells. Biochemistry 14, 2214-2218
24. Weissman, A. M. (2001) Themes and variations on ubiquitylation. Nat. Rev. Mol. Cell Biol. 2, 169-178
25. Mosesson, Y., Shtiegman, K., Katz, M., Zwang, Y., Vereb, G., Szollosi, J. and Yarden, Y. (2003) Endocytosis of receptor tyrosine kinases is driven by monoubiquitylation, not polyubiquitylation. J. Biol. Chem. 278, 21323-21326
26. Mosesson, Y. and Yarden, Y. (2006) Monoubiquitylation: a recurrent theme in membrane protein transport. Isr. Med Assoc. J. 8, 233-237
27. Pickart, C. M. (2001) Mechanisms underlying ubiquitination. Annu. Rev. Biochem. 70, 503-533
28. Yokouchi, M., Kondo, T., Houghton, A., Bartkiewicz, M., Horne, W. C., Zhang, H., Yoshimura, A. and Baron, R. (1999) Ligand-induced ubiquitination of the epidermal growth factor receptor involves the interaction of the c-Cbl RING finger and UbcH7. J. Biol. Chem. 274, 31707-31712
29. Schmidt, M. H. and Dikic, I. (2005) The Cbl interactome and its functions. Nat. Rev. Mol. Cell Biol. 6, 907-918
30. Kim, K. T., Choi, H. H., Steinmetz, M. O., Maco, B., Kammerer, R. A., Ahn, S. Y., Kim, H. Z., Lee, G. M. and Koh, G. Y. (2005) Oligomerization and multimerization are critical for angiopoietin-1 to bind and phosphorylate Tie2. J. Biol. Chem. 280, 20126-20131
31. Jones, N. and Dumont, D. J. (1998) The Tek/Tie2 receptor signals through a novel Dok-related docking protein, Dok-R. Oncogene 17, 1097-1108
32. Swaminathan, G. and Tsygankov, A. Y. (2006) The Cbl family proteins: ring leaders in regulation of cell signaling. J. Cell Physiol. 209, 21-43
33. Acconcia, F., Sigismund, S. and Polo, S. (2009) Ubiquitin in trafficking: the network at work. Exp. Cell. Res. 315, 1610-1618
34. Yabkowitz, R., Meyer, S., Yanagihara, D., Brankow, D., Staley, T., Elliott, G., Hu, S. and Ratzkin, B. (1997) Regulation of tie receptor expression on human endothelial cells by protein kinase C-mediated release of soluble tie. Blood 90, 706-715
35. Sorkin, A., Helin, K., Waters, C. M., Carpenter, G. and Beguinot, L. (1992) Multiple autophosphorylation sites of the epidermal growth factor receptor are essential for receptor kinase activity and internalization. Contrasting significance of tyrosine 992 in the native and truncated receptors. J. Biol. Chem. 267, 8672-8678
36. Duval, M., Bedard-Goulet, S., Delisle, C. and Gratton, J. P. (2003) Vascular endothelial growth factor-dependent down-regulation of Flk-1/ KDR involves Cbl-mediated ubiquitination. Consequences on nitric oxide production from endothelial cells. J. Biol. Chem. 278, 20091-20097
37. Kobayashi, S., Sawano, A., Nojima, Y., Shibuya, M. and Maru, Y. (2004) The c-Cbl/CD2AP complex regulates VEGF-induced endocytosis and degradation of Flt-1 (VEGFR-1). FASEB J. 18, 929-931
38. Holmqvist, K., Welsh, M. and Lu, L. (2005) A role of the protein Cbl in FGF-2-induced angiogenesis in murine brain endothelial cells. Cell Signal. 17, 1433-1438
39. Augustin, H. G., Koh, G. Y., Thurston, G. and Alitalo, K. (2009) Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat. Rev. Mol. Cell Biol. 10, 165-177