Anti-human activin receptor-like kinase 1 (ALK1) antibody attenuates bone morphogenetic protein 9 (BMP9)-induced ALK1 signaling and interferes with endothelial cell sprouting

Journal of Biological Chemistry

Volumn 287, Issue 22, 2012, Pages 18551-18561

  Van Meeteren, Laurens A ^a   Thorikay, Midory ^a   Bergqvist, Simon ^b   Pardali, Evangelia ^c   Stampino, Corrado Gallo ^d   Hu Lowe, Dana ^b   Goumans, Marie José ^a   Ten Dijke, Peter ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b PFIZER INC   (United States)

^c UNIVERSITY OF MÜNSTER   (Germany)

^d ICE Srl   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; ANTI-ANGIOGENIC ACTIVITY; ANTIANGIOGENESIS; ATTRACTIVE STRATEGIES; BONE MORPHOGENETIC PROTEINS; CANCER THERAPY; CLINICAL TRIAL; ENDOGLIN; MECHANISM OF ACTION; RECEPTOR-LIKE KINASE; SIGNALING COMPLEX; TRANSFORMING GROWTH FACTORS; VASCULAR DEVELOPMENT; VASCULAR ENDOTHELIAL GROWTH FACTOR;

ANTIBODIES; ENZYMES; GLYCOPROTEINS; SIGNALING;

ENDOTHELIAL CELLS;

ACTIVIN RECEPTOR LIKE KINASE 1; ACTIVIN RECEPTOR LIKE KINASE 1 ANTIBODY; ANGIOGENESIS INHIBITOR; BONE MORPHOGENETIC PROTEIN 9; ENDOGLIN; ENZYME ANTIBODY; PF 03446962; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR;

ANGIOGENESIS; ANIMAL CELL; ANTIANGIOGENIC ACTIVITY; ARTICLE; CELL MATURATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ANALYSIS; ENZYME BINDING; HUMAN; HUMAN CELL; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ACTIVIN RECEPTORS, TYPE II; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; FLOW CYTOMETRY; GROWTH DIFFERENTIATION FACTOR 2; HUMANS; POLYMERASE CHAIN REACTION; PROTEIN BINDING; SIGNAL TRANSDUCTION;

EID: 84861557944     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.338103     Document Type: Article

References (40)

1. Carmeliet, P., and Jain, R. K. (2011) Molecular mechanisms and clinical applications of angiogenesis. Nature 473, 298-307
2. van Meeteren, L. A., and ten Dijke, P. (2012) Regulation of endothelial cell plasticity by TGF-β. Cell Tissue Res. 347, 177-186
3. Goumans, M. J., Valdimarsdottir, G., Itoh, S., Lebrin, F., Larsson, J., Mummery, C., Karlsson, S., and ten Dijke, P. (2003) Activin receptor-like kinase (ALK)1 is an antagonistic mediator of lateral TGFβ/ALK5 signaling. Mol. Cell 12, 817-828 (Pubitemid 37352776)
4. Valdimarsdottir, G., Goumans, M. J., Rosendahl, A., Brugman, M., Itoh, S., Lebrin, F., Sideras, P., and ten Dijke, P. (2002) Stimulation of Id1 expression by bone morphogenetic protein is sufficient and necessary for bone morphogenetic protein-induced activation of endothelial cells. Circulation 106, 2263-2270 (Pubitemid 35222223)
5. Roelen, B. A., van Rooijen, M. A., and Mummery, C. L. (1997) Expression of ALK-1, a type 1 serine/threonine kinase receptor, coincides with sites of vasculogenesis and angiogenesis in early mouse development. Dev. Dyn. 209, 418-430 (Pubitemid 27328468)
6. Wu, X., Robinson, C. E., Fong, H. W., Crabtree, J. S., Rodriguez, B. R., Roe, B. A., and Gimble, J. M. (1995) Cloning and characterization of the murine activin receptor like kinase-1 (ALK-1) homolog. Biochem. Biophys. Res. Commun. 216, 78-83
7. Seki, T., Hong, K. H., and Oh, S. P. (2006) Nonoverlapping expression patterns of ALK1 and ALK5 reveal distinct roles of each receptor in vascular development. Lab. Invest. 86, 116-129 (Pubitemid 43117592)
8. Urness, L. D., Sorensen, L. K., and Li, D. Y. (2000) Arteriovenous malformations in mice lacking activin receptor-like kinase-1. Nat. Genet. 26, 328-331
9. Oh, S. P., Seki, T., Goss, K. A., Imamura, T., Yi, Y., Donahoe, P. K., Li, L., Miyazono, K., ten Dijke, P., Kim, S., and Li, E. (2000) Activin receptor-like kinase 1 modulates transforming growth factor-β1 signaling in the regulation of angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 97, 2626-2631 (Pubitemid 30159221)
10. Park, S. O., Wankhede, M., Lee, Y. J., Choi, E. J., Fliess, N., Choe, S. W., Oh, S. H., Walter, G., Raizada, M. K., Sorg, B. S., and Oh, S. P. (2009) Real-time imaging of de novo arteriovenous malformation in a mouse model of hereditary hemorrhagic telangiectasia. J. Clin. Investig. 119, 3487-3496
11. Niessen, K., Zhang, G., Ridgway, J. B., Chen, H., and Yan, M. (2010) ALK1 signaling regulates early postnatal lymphatic vessel development. Blood 115, 1654-1661
12. Roman, B. L., Pham, V. N., Lawson, N. D., Kulik, M., Childs, S., Lekven, A. C., Garrity, D. M., Moon, R. T., Fishman, M. C., Lechleider, R. J., and Weinstein, B. M. (2002) Disruption of acvrl1 increases endothelial cell number in zebrafish cranial vessels. Development 129, 3009-3019 (Pubitemid 34874278)
13. Johnson, D. W., Berg, J. N., Baldwin, M. A., Gallione, C. J., Marondel, I., Yoon, S. J., Stenzel, T. T., Speer, M., Pericak-Vance, M. A., Diamond, A., Guttmacher, A. E., Jackson, C. E., Attisano, L., Kucherlapati, R., Porteous, M. E., and Marchuk, D. A. (1996) Mutations in the activin receptor-like kinase 1 gene in hereditary haemorrhagic telangiectasia type 2. Nat. Genet. 13, 189-195
14. McAllister, K. A., Grogg, K. M., Johnson, D. W., Gallione, C. J., Baldwin, M. A., Jackson, C. E., Helmbold, E. A., Markel, D. S., McKinnon, W. C., and Murrell, J. (1994) Endoglin, a TGF-β binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nat. Genet. 8, 345-351
15. Castonguay, R., Werner, E. D., Matthews, R. G., Presman, E., Mulivor, A. W., Solban, N., Sako, D., Pearsall, R. S., Underwood, K. W., Seehra, J., Kumar, R., and Grinberg, A. V. (2011) Soluble endoglin specifically binds bone morphogenetic proteins 9 and 10 via its orphan domain, inhibits blood vessel formation, and suppresses tumor growth. J. Biol. Chem. 286, 30034-30046
16. Blanco, F. J., Santibanez, J. F., Guerrero-Esteo, M., Langa, C., Vary, C. P., and Bernabeu, C. (2005) Interaction and functional interplay between endoglin and ALK-1, two components of the endothelial transforming growth factor-β receptor complex. J. Cell. Physiol. 204, 574-584 (Pubitemid 40934653)
17. van Meeteren, L. A., Goumans, M. J., and Ten Dijke, P. (2011) TGF-βreceptor signaling pathways in angiogenesis; emerging targets for antiangiogenesis therapy. Curr. Pharm. Biotechnol. 12, 2108-2120
18. Mitchell, D., Pobre, E. G., Mulivor, A. W., Grinberg, A. V., Castonguay, R., Monnell, T. E., Solban, N., Ucran, J. A., Pearsall, R. S., Underwood, K. W., Seehra, J., and Kumar, R. (2010) ALK1-Fc inhibits multiple mediators of angiogenesis and suppresses tumor growth. Mol. Cancer Ther. 9, 379-388
19. Cunha, S. I., Pardali, E., Thorikay, M., Anderberg, C., Hawinkels, L., Goumans, M. J., Seehra, J., Heldin, C. H., ten Dijke, P., and Pietras, K. (2010) Genetic and pharmacological targeting of activin receptor-like kinase 1 impairs tumor growth and angiogenesis. J. Exp. Med. 207, 85-100
20. Kellermann, S. A., and Green, L. L. (2002) Antibody discovery: the use of transgenic mice to generate human monoclonal antibodies for therapeutics. Curr. Opin. Biotechnol. 13, 593-597
21. Hu-Lowe, D., Wickman, G., Jiang, X., Kraynov, E., Wang, J., Amundson, K., Simmons, B., Liang, S., Chen, E., Karlicek, S., Thompson, J., Swanson, T., Yan, Z., Li, G., Los, G., Hostomsky, Z., Casperson, G., Bender, S., and North, M. (2009) in Proceedings of the 100th Annual Meeting of the American Association for Cancer Research, Denver, April 18-22, 2009 (Abstr. 2007), American Association for Cancer Research, Philadelphia
22. Mancuso, P., Shalinsky, D. R., Calleri, A., Quarna, J., Antoniotti, P., Jilani, I., Hu-Lowe, D., Jiang, X., Gallo-Stampino, C., and Bertolini, F. (2009) Evaluation of ALK-1 expression in circulating endothelial cells (CECs) as an exploratory biomarker for PF-03446962 undergoing phase I trial in cancer patients. J. Clin. Oncol. 27, 15s (suppl; abstr 3573)
23. Goff, L. W., De Braud, F. G., Cohen, R. B., Berlin, J., Noberasco, C., Borghaei, H., Wang, E., Hu-Lowe, D., Levin, W. J., and Gallo-Stampino, C. (2010) Phase I study of PF-03446962, a fully human mab against ALK1, a TGFβ receptor involved in tumor angiogenesis. J. Clin. Oncol. 28, 15s (suppl; abstr 3034)
24. Persson, U., Izumi, H., Souchelnytskyi, S., Itoh, S., Grimsby, S., Engström, U., Heldin, C. H., Funa, K., and ten Dijke, P. (1998) The L45 loop in type I receptors for TGF-β family members is a critical determinant in specifying Smad isoform activation. FEBS Lett. 434, 83-87 (Pubitemid 28404667)
25. Korchynskyi, O., and ten Dijke, P. (2002) Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J. Biol. Chem. 277, 4883-4891 (Pubitemid 34968524)
26. Ebisawa, T., Tada, K., Kitajima, I., Tojo, K., Sampath, T. K., Kawabata, M., Miyazono, K., and Imamura, T. (1999) Characterization of bone morphogenetic protein-6 signaling pathways in osteoblast differentiation. J. Cell Sci. 112, 3519-3527
27. Nakatsu, M. N., Davis, J., and Hughes, C. C. (2007) Optimized fibrin gel bead assay for the study of angiogenesis. J. Vis. Exp. 3, 186
28. Hughes, C. C. (2007) Christopher Hughes: an in vitro model for the study of angiogenesis (interview). J. Vis. Exp. 3, 175
29. Frolik, C. A., Wakefield, L. M., Smith, D. M., and Sporn, M. B. (1984) Characterization of a membrane receptor for transforming growth factor-βin normal rat kidney fibroblasts. J. Biol. Chem. 259, 10995-11000 (Pubitemid 14030183)
30. Yamashita, H., ten Dijke, P., Huylebroeck, D., Sampath, T. K., Andries, M., Smith, J. C., Heldin, C. H., and Miyazono, K. (1995) Osteogenic protein-1 binds to activin type II receptors and induces certain activin-like effects. J. Cell Biol. 130, 217-226
31. Scharpfenecker, M., van Dinther, M., Liu, Z., van Bezooijen, R. L., Zhao, Q., Pukac, L., Löwik, C. W., and ten Dijke, P. (2007) BMP-9 signals via ALK1 and inhibits bFGF-induced endothelial cell proliferation and VEGF-stimulated angiogenesis. J. Cell Sci. 120, 964-972 (Pubitemid 46638511)
32. Goumans, M. J., Valdimarsdottir, G., Itoh, S., Rosendahl, A., Sideras, P., and ten Dijke, P. (2002) Balancing the activation state of the endothelium via two distinct TGF-β type I receptors. EMBO J. 21, 1743-1753 (Pubitemid 34614630)
33. David, L., Mallet, C., Keramidas, M., Lamandé, N., Gasc, J. M., Dupuis- Girod, S., Plauchu, H., Feige, J. J., and Bailly, S. (2008) Bone morphogenetic protein-9 is a circulating vascular quiescence factor. Circ. Res. 102, 914-922 (Pubitemid 351591550)
34. Suzuki, Y., Ohga, N., Morishita, Y., Hida, K., Miyazono, K., and Watabe, T. (2010) BMP-9 induces proliferation of multiple types of endothelial cells in vitro and in vivo. J. Cell Sci. 123, 1684-1692
35. Scotti, C., Olivieri, C., Boeri, L., Canzonieri, C., Ornati, F., Buscarini, E., Pagella, F., and Danesino, C. (2011) Bioinformatic analysis of pathogenic missense mutations of activin receptor like kinase 1 ectodomain. PLoS One 6, e26431
36. David, L., Mallet, C., Mazerbourg, S., Feige, J. J., and Bailly, S. (2007) Identification of BMP9 and BMP10 as functional activators of the orphan activin receptor-like kinase 1 (ALK1) in endothelial cells. Blood 109, 1953-1961 (Pubitemid 46348192)
37. Brown, M. A., Zhao, Q., Baker, K. A., Naik, C., Chen, C., Pukac, L., Singh, M., Tsareva, T., Parice, Y., Mahoney, A., Roschke, V., Sanyal, I., and Choe, S. (2005) Crystal structure of BMP-9 and functional interactions with pro-region and receptors. J. Biol. Chem. 280, 25111-25118 (Pubitemid 40934603)
38. Larrivée, B., Prahst, C., Gordon, E., Del Toro, R., Mathivet, T., Duarte, A., Simons, M., and Eichmann, A. (2012) ALK1 signaling inhibits angiogenesis by cooperating with the Notch pathway. Dev. Cell 22, 489-500
39. Seehra, J., Knopf, J., Pearsall, R. S., Grinberg, A., and Kumar, R. (November 19, 2009) International Patent WO2009139891
40. North, M. A., Amundson, K. K., Bedian, V., Belouski, S. S., Hu-Lowe, D. D., Jiang, X., Karlicek, S. M., Kellermann, S.-A., Thomson, J. A., Wang, J., Wickman, G. R., and Zhang, J. (April 21, 2007) International Patent WO2007040912