Src-mediated post-translational regulation of endoglin stability and function is critical for angiogenesis

Journal of Biological Chemistry

Volumn 289, Issue 37, 2014, Pages 25486-25496

  Pan, Christopher C ^a   Kumar, Sanjay ^a   Shah, Nirav ^a   Hoyt, Dale G ^a   Hawinkels, Lukas J A C ^d   Mythreye, Karthikeyan ^c   Lee, Nam Y ^a,b  

^a Division of Pharmacology College of Pharmacy ^*  (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF SOUTH CAROLINA   (United States)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ENDOTHELIAL CELLS; ENZYME INHIBITION;

CRITICAL DETERMINANT; ENDOTHELIAL FUNCTION; EPIDERMAL GROWTH FACTORS; RECEPTOR-LIKE KINASE; TRANSFORMING GROWTH FACTOR BETA; TRANSLATIONAL REGULATION; TUMOR VASCULARIZATION; VASCULAR ENDOTHELIAL GROWTH FACTOR;

PHOSPHORYLATION;

ENDOGLIN; EPIDERMAL GROWTH FACTOR; PROTEIN ANTIBODY; PROTEIN TYROSINE KINASE; VASCULOTROPIN; ACTIVIN RECEPTOR 2; ACVRL1 PROTEIN, HUMAN; CELL SURFACE RECEPTOR; ENG PROTEIN, HUMAN; LEUKOCYTE ANTIGEN; PROTEIN SERINE THREONINE KINASE; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR-BETA TYPE II RECEPTOR;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CAPILLARY TUBE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DEGRADATION; DOWN REGULATION; EMBRYO; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; INTERNALIZATION; LYSOSOME; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN STRUCTURE; CYTOLOGY; GENETICS; METABOLISM; PHOSPHORYLATION;

ACTIVIN RECEPTORS, TYPE II; AMINO ACID MOTIFS; ANTIGENS, CD; CELL PROLIFERATION; ENDOTHELIAL CELLS; HUMANS; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHORYLATION; PROTEIN STABILITY; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CELL SURFACE; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SRC-FAMILY KINASES; TRANSFORMING GROWTH FACTOR BETA;

EID: 84907164678     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.578609     Document Type: Article

References (40)

1. Massague, J., and Chen, Y. G. (2000) Controlling TGF-β signaling. Genes Dev. 14, 627-644
2. Ehrlich, M., Gutman, O., Knaus, P., and Henis, Y. I. (2012) Oligomeric interactions of TGF-β and BMP receptors. FEBS Letters 586, 1885-1896
3. Ehrlich, M., Horbelt, D., Marom, B., Knaus, P., and Henis, Y. I. (2011) Homomeric and heteromeric complexes among TGF-β and BMP receptors and their roles in signaling. Cell. Signal. 23, 1424-1432
4. Derynck, R., and Zhang, Y. E. (2003) Smad-dependent and Smad-independent pathways in TGF-β family signalling. Nature 425, 577-584
5. Huang, F., and Chen, Y. G. (2012) Regulation of TGF-β receptor activity. Cell Bioscience 2, 9
6. Ikushima, H., and Miyazono, K. (2010) TGFβ signalling: a complex web in cancer progression. Nature Reviews. Cancer 10, 415-424
7. Massague, J., Seoane, J., and Wotton, D. (2005) Smad transcription factors. Genes Dev. 19, 2783-2810
8. Lebrin, F., Deckers, M., Bertolino, P., and Ten Dijke, P. (2005) TGF-β receptor function in the endothelium. Cardiovasc. Res. 65, 599-608
9. Barbara, N. P., Wrana, J. L., and Letarte, M. (1999) Endoglin is an accessory protein that interacts with the signaling receptor complex of multiple members of the transforming growth factor-β superfamily. J. Biol. Chem. 274, 584-594
10. Lebrin, F., Goumans, M. J., Jonker, L., Carvalho, R. L. C., Valdimarsdottir, G., Thorikay, M., Mummery, C., Arthur, H. M., and ten Dijke, P. (2004) Endoglin promotes endothelial cell proliferation and TGF-β/ALK1 signal transduction. EMBO J. 23, 4018-4028
11. Nassiri, F., Cusimano, M. D., Scheithauer, B. W., Rotondo, F., Fazio, A., Yousef, G. M., Syro, L. V., Kovacs, K., and Lloyd, R. V. (2011) Endoglin (CD105): a review of its role in angiogenesis and tumor diagnosis, progression and therapy. Anticancer Res. 31, 2283-2290
12. Bernabeu, C., Conley, B. A., and Vary, C. P. (2007) Novel biochemical pathways of endoglin in vascular cell physiology. J. Cell. Biochem. 102, 1375-1388
13. López-Novoa, J. M., and Bernabeu, C. (2010) The physiological role of endoglin in the cardiovascular system. Am. J. Physiol. Heart and Circulatory Physiology 299, H959-H974
14. Bernabeu, C., Lopez-Novoa, J. M., and Quintanilla, M. (2009) The emerging role of TGF-β superfamily coreceptors in cancer. Biochim. Biophys. Acta 1792, 954-973
15. Pérez-Gómez, E., Del Castillo, G., Juan Francisco, S., López-Novoa, J. M., Bernabéu, C., and Quintanilla, M. (2010) The role of the TGF-β coreceptor endoglin in cancer. The Scientific World Journal 10, 2367-2384
16. Rosen, L. S., Hurwitz, H. I., Wong, M. K., Goldman, J., Mendelson, D. S., Figg, W. D., Spencer, S., Adams, B. J., Alvarez, D., Seon, B. K., Theuer, C. P., Leigh, B. R., and Gordon, M. S. (2012) A Phase I First-in-Human Study of TRC105 (Anti-Endoglin Antibody) in Patients with Advanced Cancer. Clinical Cancer Res. 18, 4820-4829
17. Weis, S. M., and Cheresh, D. A. (2011) Tumor angiogenesis: molecular pathways and therapeutic targets. Nat. Med. 17, 1359-1370
18. Fonsatti, E., Nicolay, H. J., Altomonte, M., Covre, A., and Maio, M. (2010) Targeting cancer vasculature via endoglin/CD105: a novel antibody-based diagnostic and therapeutic strategy in solid tumours. Cardiovasc. Res. 86, 12-19
19. Lee, N. Y., and Blobe, G. C. (2007) The interaction of endoglin with β-arrestin2 regulates transforming growth factor-β-mediated ERK activation and migration in endothelial cells. J. Biol. Chem. 282, 21507-21517
20. Meng, Q., Lux, A., Holloschi, A., Li, J., Hughes, J. M., Foerg, T., McCarthy, J. E., Heagerty, A. M., Kioschis, P., Hafner, M., and Garland, J. M. (2006) Identification of Tctex2β, a novel dynein light chain family member that interacts with different transforming growth factor-β receptors. J. Biol. Chem. 281, 37069-37080
21. Ray, B. N., Lee, N. Y., How, T., and Blobe, G. C. (2010) ALK5 phosphorylation of the endoglin cytoplasmic domain regulates Smad1/5/8 signaling and endothelial cell migration. Carcinogenesis 31, 435-441
22. Koleva, R. I., Conley, B. A., Romero, D., Riley, K. S., Marto, J. A., Lux, A., and Vary, C. P. (2006) Endoglin structure and function: Determinants of endoglin phosphorylation by transforming growth factor-β receptors. J. Biol. Chem. 281, 25110-25123
23. Tang, H., Low, B., Rutherford, S. A., and Hao, Q. (2005) Thrombin induces endocytosis of endoglin and type-II TGF-β receptor and down-regulation of TGF-β signaling in endothelial cells. Blood 105, 1977-1985
24. Lee, N. Y., Golzio, C., Gatza, C. E., Sharma, A., Katsanis, N., and Blobe, G. C. (2012) Endoglin regulates PI3-kinase/Akt trafficking and signaling to alter endothelial capillary stability during angiogenesis. Mol. Biol. Cell 23, 2412-2423
25. Pece-Barbara, N., Vera, S., Kathirkamathamby, K., Liebner, S., Di Guglielmo, G. M., Dejana, E., Wrana, J. L., and Letarte, M. (2005) Endoglin null endothelial cells proliferate faster and are more responsive to transforming growth factor β1 with higher affinity receptors and an activated Alk1 pathway. J. Biol. Chem. 280, 27800-27808
26. Hawinkels, L. J., Kuiper, P., Wiercinska, E., Verspaget, H. W., Liu, Z., Pardali, E., Sier, C. F., and ten Dijke, P. (2010) Matrix metalloproteinase-14 (MT1-MMP)-mediated endoglin shedding inhibits tumor angiogenesis. Cancer Res. 70, 4141-4150
27. Okada, M. (2012) Regulation of the SRC family kinases by Csk. Int. J. Biol. Sci. 8, 1385-1397
28. Lam, K. S., Wu, J. Z., and Lou, Q. (1995) Identification and Characterization of a Novel Synthetic Peptide Substrate-Specific for Src-Family Protein-Tyrosine Kinases. Int. J. Pept. Prot. Res. 45, 587-592
29. Schliess, F., Reissmann, R., Reinehr, R., vom Dahl, S., and Häussinger, D. (2004) Involvement of integrins and Src in insulin signaling toward autophagic proteolysis in rat liver. J. Biol. Chem. 279, 21294-21301
30. Park, S. S., Eom, Y. W., Kim, E. H., Lee, J. H., Min, D. S., Kim, S., Kim, S. J., and Choi, K. S. (2004) Involvement of c-Src kinase in the regulation of TGF-β1-induced apoptosis. Oncogene 23, 6272-6281
31. Tsujie, M., Tsujie, T., Toi, H., Uneda, S., Shiozaki, K., Tsai, H., and Seon, B. K. (2008) Anti-tumor activity of an anti-endoglin monoclonal antibody is enhanced in immunocompetent mice. Int. J. Cancer 122, 2266-2273
32. Tsujie, M., Uneda, S., Tsai, H., and Seon, B. K. (2006) Effective anti-angiogenic therapy of established tumors in mice by naked anti-human endoglin (CD105) antibody: Differences in growth rate and therapeutic response between tumors growing at different sites. Int. J. Oncol. 29, 1087-1094
33. Lee, N. Y., Ray, B., How, T., and Blobe, G. C. (2008) Endoglin promotes transforming growth factor β-mediated Smad 1/5/8 signaling and inhibits endothelial cell migration through its association with GIPC. J. Biol. Chem. 283, 32527-32533
34. Lamalice, L., Le Boeuf, F., and Huot, J. (2007) Endothelial cell migration during angiogenesis. Circ. Res. 100, 782-794
35. Li, C., Guo, B., Ding, S., Rius, C., Langa, C., Kumar, P., Bernabeu, C., and Kumar, S. (2003) TNFα down-regulates CD105 expression in vascular endothelial cells: a comparative study with TGF β1. Anticancer Res. 23, 1189-1196
36. Mitchell, H., Choudhury, A., Pagano, R. E., and Leof, E. B. (2004) Liganddependent and -independent transforming growth factor-β receptor recycling regulated by clathrin-mediated endocytosis and Rab11. Mol. Biol. Cell 15, 4166-4178
37. Takahashi, T., Takahashi, K., St John, P. L., Fleming, P. A., Tomemori, T., Watanabe, T., Abrahamson, D. R., Drake, C. J., Shirasawa, T., and Daniel, T. O. (2003) A mutant receptor tyrosine phosphatase, CD148, causes defects in vascular development. Mol. Cell. Biol. 23, 1817-1831
38. Chen, Y. G. (2009) Endocytic regulation of TGF-β signaling. Cell Res. 19, 58-70
39. Kowanetz, M., Lönn, P., Vanlandewijck, M., Kowanetz, K., Heldin, C. H., and Moustakas, A. (2008) TGFβ induces SIK to negatively regulate type I receptor kinase signaling. J. Cell Biol. 182, 655-662
40. Lönn, P., Vanlandewijck, M., Raja, E., Kowanetz, M., Watanabe, Y., Kowanetz, K., Vasilaki, E., Heldin, C. H., and Moustakas, A. (2012) Transcriptional induction of salt-inducible kinase 1 by transforming growth factorβ leads to negative regulation of type I receptor signaling in cooperation with the Smurf2 ubiquitin ligase. J. Biol. Chem. 287, 12867-12878