Regulation of bone morphogenetic protein 9 (BMP9) by redox-dependent proteolysis

Journal of Biological Chemistry

Volumn 289, Issue 45, 2014, Pages 31150-31159

  Wei, Zhenquan ^a,b   Salmon, Richard M ^a   Upton, Paul D ^a   Morrell, Nicholas W ^a   Li, Wei ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEINS;

ACTIVIN RECEPTOR LIKE KINASE 1; BONE MORPHOGENETIC PROTEIN 9; PROTEINASE; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; COMPLEMENTARY DNA; DISULFIDE; GDF2 PROTEIN, HUMAN; GDF2 PROTEIN, MOUSE; GROWTH DIFFERENTIATION FACTOR; LIGAND; RECOMBINANT PROTEIN;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DISULFIDE BOND; HOMEOSTASIS; MAMMAL CELL; OXIDATION REDUCTION POTENTIAL; PROTEIN BINDING; PROTEIN BLOOD LEVEL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; PROTEIN STABILITY; STRUCTURE ACTIVITY RELATION; VASCULAR ENDOTHELIUM; ANIMAL; CELL LINE; CHEMISTRY; CRYSTALLIZATION; CYTOLOGY; DIMERIZATION; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; HUMAN; METABOLISM; MOUSE; OXIDATION REDUCTION REACTION; PHENOTYPE; SIGNAL TRANSDUCTION; X RAY CRYSTALLOGRAPHY;

ANIMALS; CELL LINE; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; DISULFIDES; DNA, COMPLEMENTARY; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; GROWTH DIFFERENTIATION FACTOR 2; GROWTH DIFFERENTIATION FACTORS; HUMANS; LIGANDS; MICE; OXIDATION-REDUCTION; PHENOTYPE; PROTEOLYSIS; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

EID: 84909983092     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.579771     Document Type: Article

References (52)

1. 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
2. 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
3. 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
4. Liu, F., Ventura, F., Doody, J., and Massagué, J. (1995) Human type II receptor for bone morphogenic proteins (BMPs): extension of the two-kinase receptor model to the BMPs. Mol. Cell Biol. 15, 3479-3486
5. 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-β 1 signaling in the regulation of angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 97, 2626-2631
6. Beppu, H., Kawabata, M., Hamamoto, T., Chytil, A., Minowa, O., Noda, T., and Miyazono, K. (2000) BMP type II receptor is required for gastrulation and early development of mouse embryos. Dev. Biol. 221, 249-258
7. Ricard, N., Bidart, M., Mallet, C., Lesca, G., Giraud, S., Prudent, R., Feige, J. J., and Bailly, S. (2010) Functional analysis of the BMP9 response of ALK1 mutants from HHT2 patients: a diagnostic tool for novel ACVRL1 mutations. Blood 116, 1604-1612
8. Wooderchak-Donahue, W. L., McDonald, J., O'Fallon, B., Upton, P. D., Li, W., Roman, B. L., Young, S., Plant, P., Fülöp, G. T., Langa, C., Morrell, N. W., Botella, L. M., Bernabeu, C., Stevenson, D. A., Runo, J. R., and Bayrak-Toydemir, P. (2013) BMP9 mutations cause a vascular-anomaly syndrome with phenotypic overlap with hereditary hemorrhagic telangiectasia. Am. J. Hum. Genet. 93, 530-537
9. International PPH Consortium, Lane, K. B., Machado, R. D., Pauciulo, M. W., Thomson, J. R., Phillips, J. A., 3rd, Loyd, J. E., Nichols, W. C., and Trembath, R. C. (2000) Heterozygous germline mutations in BMPR2, encoding a TGF-β receptor, cause familial primary pulmonary hypertension. Nat. Genet. 26, 81-84
10. Morrell, N. W. (2006) Pulmonary hypertension due to BMPR2 mutation: a new paradigm for tissue remodeling? Proc. Am. Thorac. Soc. 3, 680-686
11. Trembath, R. C., Thomson, J. R., Machado, R. D., Morgan, N. V., Atkinson, C., Winship, I., Simonneau, G., Galie, N., Loyd, J. E., Humbert, M., Nichols, W. C., Morrell, N. W., Berg, J., Manes, A., McGaughran, J., Pauciulo, M., and Wheeler, L. (2001) Clinical and molecular genetic features of pulmonary hypertension in patients with hereditary hemorrhagic telangiectasia. N. Engl. J. Med. 345, 325-334
12. Harrison, R. E., Flanagan, J. A., Sankelo, M., Abdalla, S. A., Rowell, J., Machado, R. D., Elliott, C. G., Robbins, I. M., Olschewski, H., McLaughlin, V., Gruenig, E., Kermeen, F., Halme, M., Räisänen-Sokolowski, A., Laitinen, T., Morrell, N. W., and Trembath, R. C. (2003) Molecular and functional analysis identifies ALK-1 as the predominant cause of pulmonary hypertension related to hereditary haemorrhagic telangiectasia. J. Med. Genet. 40, 865-871
13. Jerkic, M., Kabir, M. G., Davies, A., Yu, L. X., McIntyre, B. A., Husain, N. W., Enomoto, M., Sotov, V., Husain, M., Henkelman, M., Belik, J., and Letarte, M. (2011) Pulmonary hypertension in adult Alk1 heterozygous mice due to oxidative stress. Cardiovasc. Res. 92, 375-384
14. Burton, V. J., Ciuclan, L. I., Holmes, A. M., Rodman, D. M., Walker, C., and Budd, D. C. (2011) Bone morphogenetic protein receptor II regulates pulmonary artery endothelial cell barrier function. Blood 117, 333-341
15. Burton, V. J., Holmes, A. M., Ciuclan, L. I., Robinson, A., Roger, J. S., Jarai, G., Pearce, A. C., and Budd, D. C. (2011) Attenuation of leukocyte recruitment via CXCR1/2 inhibition stops the progression of PAH in mice with genetic ablation of endothelial BMPR-II. Blood 118, 4750-4758
16. Teichert-Kuliszewska, K., Kutryk, M. J., Kuliszewski, M. A., Karoubi, G., Courtman, D. W., Zucco, L., Granton, J., and Stewart, D. J. (2006) Bone morphogenetic protein receptor-2 signaling promotes pulmonary arterial endothelial cell survival: implications for loss-of-function mutations in the pathogenesis of pulmonary hypertension. Circ. Res. 98, 209-217
17. Reynolds, A. M., Holmes, M. D., Danilov, S. M., and Reynolds, P. N. (2012) Targeted gene delivery of BMPR2 attenuates pulmonary hypertension. Eur. Respir. J. 39, 329-343
18. Bidart, M., Ricard, N., Levet, S., Samson, M., Mallet, C., David, L., Subileau, M., Tillet, E., Feige, J. J., and Bailly, S. (2012) BMP9 is produced by hepatocytes and circulates mainly in an active mature form complexed to its prodomain. Cell Mol. Life Sci. 69, 313-324
19. Herrera, B., and Inman, G. J. (2009) A rapid and sensitive bioassay for the simultaneous measurement of multiple bone morphogenetic proteins. Identification and quantification of BMP4, BMP6 and BMP9 in bovine and human serum. BMC Cell Biol. 10, 20
20. Thomas, G. (2002) Furin at the cutting edge: from protein traffic to embryogenesis and disease. Nat. Rev. Mol. Cell Biol. 3, 753-766
21. Dunmore, B. J., Drake, K. M., Upton, P. D., Toshner, M. R., Aldred, M. A., and Morrell, N. W. (2013) The lysosomal inhibitor, chloroquine, increases cell surface BMPR-II levels and restores BMP9 signalling in endothelial cells harbouring BMPR-II mutations. Hum. Mol. Genet. 22, 3667-3679
22. Upton, P. D., Davies, R. J., Trembath, R. C., and Morrell, N. W. (2009) Bone morphogenetic protein (BMP) and activin type II receptors balance BMP9 signals mediated by activin receptor-like kinase-1 in human pulmonary artery endothelial cells. J. Biol. Chem. 284, 15794-15804
23. Kang, Q., Sun, M. H., Cheng, H., Peng, Y., Montag, A. G., Deyrup, A. T., Jiang, W., Luu, H. H., Luo, J., Szatkowski, J. P., Vanichakarn, P., Park, J. Y., Li, Y., Haydon, R. C., and He, T. C. (2004) Characterization of the distinct orthotopic bone-forming activity of 14 BMPs using recombinant adeno-virus-mediated gene delivery. Gene Ther. 11, 1312-1320
24. Luther, G., Wagner, E. R., Zhu, G., Kang, Q., Luo, Q., Lamplot, J., Bi, Y., Luo, X., Luo, J., Teven, C., Shi, Q., Kim, S. H., Gao, J. L., Huang, E., Yang, K., Rames, R., Liu, X., Li, M., Hu, N., Liu, H., Su, Y., Chen, L., He, B. C., Zuo, G. W., Deng, Z. L., Reid, R. R., Luu, H. H., Haydon, R. C., and He, T. C. (2011) BMP-9 induced osteogenic differentiation of mesenchymal stem cells: molecular mechanism and therapeutic potential. Curr. Gene Ther. 11, 229-240
25. Ricard, N., Ciais, D., Levet, S., Subileau, M., Mallet, C., Zimmers, T. A., Lee, S. J., Bidart, M., Feige, J. J., and Bailly, S. (2012) BMP9 and BMP10 are critical for postnatal retinal vascular remodeling. Blood 119, 6162-6171
26. Yoshimatsu, Y., Lee, Y. G., Akatsu, Y., Taguchi, L., Suzuki, H. I., Cunha, S. I., Maruyama, K., Suzuki, Y., Yamazaki, T., Katsura, A., Oh, S. P., Zimmers, T. A., Lee, S. J., Pietras, K., Koh, G. Y., Miyazono, K., and Watabe, T. (2013) Bone morphogenetic protein-9 inhibits lymphatic vessel formation via activin receptor-like kinase 1 during development and cancer progression. Proc. Natl. Acad. Sci. U.S.A. 110, 18940-18945
27. van Baardewijk, L. J., van der Ende, J., Lissenberg-Thunnissen, S., Romijn, L. M., Hawinkels, L. J., Sier, C. F., and Schipper, I. B. (2013) Circulating bone morphogenetic protein levels and delayed fracture healing. Int. Orthop. 37, 523-527
28. 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
29. Luo, J., Tang, M., Huang, J., He, B. C., Gao, J. L., Chen, L., Zuo, G. W., Zhang, W., Luo, Q., Shi, Q., Zhang, B. Q., Bi, Y., Luo, X., Jiang, W., Su, Y., Shen, J., Kim, S. H., Huang, E., Gao, Y., Zhou, J. Z., Yang, K., Luu, H. H., Pan, X., Haydon, R. C., Deng, Z. L., and He, T. C. (2010) TGFβ/BMP type I receptors ALK1 and ALK2 are essential for BMP9-induced osteogenic signaling in mesenchymal stem cells. J. Biol. Chem. 285, 29588-29598
30. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., Read, R. J., Vagin, A., and Wilson, K. S. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242
31. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
32. 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
33. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
34. Murshudov, G. N., Skubák, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F., and Vagin, A. A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367
35. Afonine, P. V., Grosse-Kunstleve, R. W., Echols, N., Headd, J. J., Moriarty, N. W., Mustyakimov, M., Terwilliger, T. C., Urzhumtsev, A., Zwart, P. H., and Adams, P. D. (2012) Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr. D Biol. Crystallogr. 68, 352-367
36. Zhou, A., Carrell, R. W., Murphy, M. P., Wei, Z., Yan, Y., Stanley, P. L., Stein, P. E., Broughton Pipkin, F., and Read, R. J. (2010) A redox switch in angiotensinogen modulates angiotensin release. Nature 468, 108-111
37. Jones, W. K., Richmond, E. A., White, K., Sasak, H., Kusmik, W., Smart, J., Oppermann, H., Rueger, D. C., and Tucker, R. F. (1994) Osteogenic protein-1 (OP-1) expression and processing in Chinese hamster ovary cells: isolation of a soluble complex containing the mature and pro-domains of OP-1. Growth Factors 11, 215-225
38. Knaus, P., and Sebald, W. (2001) Cooperativity of binding epitopes and receptor chains in the BMP/TGFβ superfamily. Biol. Chem. 382, 1189-1195
39. Isaacs, M. J., Kawakami, Y., Allendorph, G. P., Yoon, B. H., Izpisua Belmonte, J. C., and Choe, S. (2010) Bone morphogenetic protein-2 and -6 heterodimer illustrates the nature of ligand-receptor assembly. Mol. Endocrinol. 24, 1469-1477
40. Townson, S. A., Martinez-Hackert, E., Greppi, C., Lowden, P., Sako, D., Liu, J., Ucran, J. A., Liharska, K., Underwood, K. W., Seehra, J., Kumar, R., and Grinberg, A. V. (2012) Specificity and structure of a high affinity activin receptor-like kinase 1 (ALK1) signaling complex. J. Biol. Chem. 287, 27313-27325
41. Kosower, N. S., Kosower, E. M., Wertheim, B., and Correa, W. S. (1969) Diamide, a new reagent for the intracellular oxidation of glutathione to the disulfide. Biochem. Biophys. Res. Commun. 37, 593-596
42. Rossi, R., Milzani, A., Dalle-Donne, I., Giustarini, D., Lusini, L., Colombo, R., and Di Simplicio, P. (2002) Blood glutathione disulfide: in vivo factor or in vitro artifact? Clin. Chem. 48, 742-753
43. Shi, M., Zhu, J., Wang, R., Chen, X., Mi, L., Walz, T., and Springer, T. A. (2011) Latent TGF-β structure and activation. Nature 474, 343-349
44. Walsh, D. W., Godson, C., Brazil, D. P., and Martin, F. (2010) Extracellular BMP-antagonist regulation in development and disease: tied up in knots. Trends Cell Biol. 20, 244-256
45. Seemann, P., Brehm, A., König, J., Reissner, C., Stricker, S., Kuss, P., Haupt, J., Renninger, S., Nickel, J., Sebald, W., Groppe, J. C., Plöger, F., Pohl, J., Schmidt-von Kegler, M., Walther, M., Gassner, I., Rusu, C., Janecke, A. R., Dathe, K., and Mundlos, S. (2009) Mutations in GDF5 reveal a key residue mediating BMP inhibition by NOGGIN. PLoS Genet. 5, e1000747
46. Yao, Y., Jumabay, M., Ly, A., Radparvar, M., Wang, A. H., Abdmaulen, R., and Boström, K. I. (2012) Crossveinless 2 regulates bone morphogenetic protein 9 in human and mouse vascular endothelium. Blood 119, 5037-5047
47. Kelley, R., Ren, R., Pi, X., Wu, Y., Moreno, I., Willis, M., Moser, M., Ross, M., Podkowa, M., Attisano, L., and Patterson, C. (2009) A concentration-dependent endocytic trap and sink mechanism converts Bmper from an activator to an inhibitor of Bmp signaling. J. Cell Biol. 184, 597-609
48. Degnin, C., Jean, F., Thomas, G., and Christian, J. L. (2004) Cleavages within the prodomain direct intracellular trafficking and degradation of mature bone morphogenetic protein-4. Mol. Biol. Cell 15, 5012-5020
49. Spoelgen, R., Hammes, A., Anzenberger, U., Zechner, D., Andersen, O. M., Jerchow, B., and Willnow, T. E. (2005) LRP2/megalin is required for patterning of the ventral telencephalon. Development 132, 405-414
50. López-Coviella, I., Berse, B., Krauss, R., Thies, R. S., and Blusztajn, J. K. (2000) Induction and maintenance of the neuronal cholinergic phenotype in the central nervous system by BMP-9. Science 289, 313-316
51. Burke, R. M., Norman, T. A., Haydar, T. F., Slack, B. E., Leeman, S. E., Blusztajn, J. K., and Mellott, T. J. (2013) BMP9 ameliorates amyloidosis and the cholinergic defect in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 110, 19567-19572
52. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21