Structure of Gremlin-1 and analysis of its interaction with BMP-2

Biochemical Journal

Volumn 473, Issue 11, 2016, Pages 1593-1604

  Kišonaite, Migle ^a   Wang, Xuelu ^a   Hyvönen, Marko ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

(TGF ); Bone morphogenetic protein (BMP); Differential screening aberrative in neuroblastoma (DAN); Extracellular antagonism; Gremlin; Structural biology; Transforming growth factor ; X ray crystallography

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; CHORDIN; GREMLIN 1; NOGGIN; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG; BMP2 PROTEIN, HUMAN; CARRIER PROTEIN; GLYCOPROTEIN; GREM1 PROTEIN, HUMAN; NOGGIN PROTEIN; PROTEIN BINDING; SIGNAL PEPTIDE;

ANIMAL CELL; ARTICLE; BINDING SITE; BIOLAYER INTERFEROMETRY; CONTROLLED STUDY; CRYSTAL STRUCTURE; INTERFEROMETRY; MOUSE; MUTAGENESIS; NONHUMAN; PHOTON CORRELATION SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; STOICHIOMETRY; ULTRACENTRIFUGATION; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MUTATION; PHYSIOLOGY; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SIGNAL TRANSDUCTION; X RAY CRYSTALLOGRAPHY;

BONE MORPHOGENETIC PROTEIN 2; CARRIER PROTEINS; CRYSTALLOGRAPHY, X-RAY; GLYCOPROTEINS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; SIGNAL TRANSDUCTION;

EID: 84975142536     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BCJ20160254     Document Type: Article

References (51)

1. Dionne, M.S., Skarnes, W.C. and Harland, R.M. (2001) Mutation and analysis of Dan, the founding member of the Dan family of transforming growth factor beta antagonists. Mol. Cell. Biol. 21, 636-643
2. Nolan, K. and Thompson, T.B. (2014) The DAN family: modulators of TGF-β signaling and beyond. Protein Sci. 23, 999-1012
3. Rider, C.C. and Mulloy, B. (2010) Bone morphogenetic protein and growth differentiation factor cytokine families and their protein antagonists. Biochem. J. 429, 1-12
4. 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
5. Allendorph, G.P., Vale, W.W. and Choe, S. (2006) Structure of the ternary signaling complex of a TGF-β superfamily member. Proc. Natl. Acad. Sci. U.S.A. 103, 7643-7648
6. Bragdon, B., Moseychuk, O., Saldanha, S., King, D., Julian, J. and Nohe, A. (2011) Bone morphogenetic proteins: a critical review. Cell. Signal. 23, 609-620
7. Chen, H., Brady Ridgway, J., Sai, T., Lai, J., Warming, S., Chen, H., Roose-Girma, M., Zhang, G., Shou, W. and Yan, M. (2013) Context-dependent signaling defines roles of BMP9 and BMP10 in embryonic and postnatal development. Proc. Natl. Acad. Sci. U.S.A. 110, 11887-11892
8. Derynck, R. and Feng, X.H. (1997) TGF-beta receptor signaling. Biochim. Biophys. Acta 1333, F105-F150
9. Harrison, C.A., Wiater, E., Gray, P.C., Greenwald, J., Choe, S. and Vale, W. (2004) Modulation of activin and BMP signaling. Mol. Cell. Endocrinol. 225, 19-24
10. Hogan, B.L. (1996) Bone morphogenetic proteins in development. Curr. Opin. Genet. Dev. 6, 432-438
11. Macias, M.J., Martin-Malpartida, P. and Massagué, J. (2015) Structural determinants of Smad function in TGF-β signaling. Trends Biochem. Sci. 40, 296-308
12. Cai, J., Pardali, E., Sánchez-Duffhues, G. and ten Dijke, P. (2012) BMP signaling in vascular diseases. FEBS Lett. 586, 1993-2002
13. Long, L., Ormiston, M.L., Yang, X., Southwood, M., Gräf, S., Machado, R.D., Mueller, M., Kinzel, B., Yung, L.M., Wilkinson, J.M. et al. (2015) Selective enhancement of endothelial BMPR-II with BMP9 reverses pulmonary arterial hypertension. Nat. Med. 21, 777-785
14. Xiao, Y.-T., Xiang, L.-X. and Shao, J.-Z. (2007) Bone morphogenetic protein. Biochem. Biophys. Res. Commun. 362, 550-553
15. Allendorph, G.P., Isaacs, M.J., Kawakami, Y., Izpisua Belmonte, J.C. and Choe, S. (2007) BMP-3 and BMP-6 structures illuminate the nature of binding specificity with receptors. Biochemistry 46, 12238-12247
16. Nickel, J., Sebald, W., Groppe, J.C. and Mueller, T.D. (2009) Intricacies of BMP receptor assembly. Cytokine Growth Factor Rev. 20, 367-377
17. Nohe, A., Hassel, S., Ehrlich, M., Neubauer, F., Sebald, W., Henis, Y.I. and Knaus, P. (2002) The mode of bone morphogenetic protein (BMP) receptor oligomerization determines different BMP-2 signaling pathways. J. Biol. Chem. 277, 5330-5338
18. Alborzinia, H., Schmidt-Glenewinkel, H., Ilkavets, I., Breitkopf-Heinlein, K., Cheng, X., Hortschansky, P., Dooley, S. and Wölfl, S. (2013) Quantitative kinetics analysis of BMP2 uptake into cells and its modulation by BMP antagonists. J. Cell Sci. 126, 117-127
19. Bier, E. (2008) Intriguing extracellular regulation of BMP signaling. Dev. Cell 15, 176-177
20. Groppe, J., Greenwald, J., Wiater, E., Rodriguez-Leon, J., Economides, A.N., Kwiatkowski, W., Affolter, M., Vale, W.W., Izpisua Belmonte, J.C. and Choe, S. (2002) Structural basis of BMP signalling inhibition by the cystine knot protein Noggin. Nature 420, 636-642
21. Yanagita, M. (2005) BMP antagonists: their roles in development and involvement in pathophysiology. Cytokine Growth Factor Rev. 16, 309-317
22. Hsu, D.R., Economides, A.N., Wang, X., Eimon, P.M. and Harland, R.M. (1998) The Xenopus dorsalizing factor Gremlin identifies a novel family of secreted proteins that antagonize BMP activities. Mol. Cell 1, 673-683
23. Müller, I., Schönberger, T., Schneider, M., Borst, O., Ziegler, M., Seizer, P., Leder, C., Müller, K., Lang, M., Appenzeller, F. et al. (2013) Gremlin-1 is an inhibitor of macrophage migration inhibitory factor and attenuates atherosclerotic plaque growth in ApoE-/- mice. J. Biol. Chem. 288, 31635-31645
24. Wellbrock, J., Harbaum, L., Stamm, H., Hennigs, J.K., Schulz, B., Klose, H., Bokemeyer, C., Fiedler, W. and Lüneburg, N. (2015) Intrinsic BMP antagonist gremlin-1 as a novel circulating marker in pulmonary arterial hypertension. Lung 193, 567-570
25. Kosinski, C., Li, V.S., Chan, A.S., Zhang, J., Ho, C., Tsui, W.Y., Chan, T.L., Mifflin, R.C., Powell, D.W., Yuen, S.T. et al. (2007) Gene expression patterns of human colon tops and basal crypts and BMP antagonists as intestinal stem cell niche factors. Proc. Natl. Acad. Sci. U.S.A. 104, 15418-15423
26. Davis, H., Irshad, S., Bansal, M., Rafferty, H., Boitsova, T., Bardella, C., Jaeger, E., Lewis, A., Freeman-Mills, L., Giner, F.C. et al. (2015) Aberrant epithelial GREM1 expression initiates colonic tumorigenesis from cells outside the stem cell niche. Nat. Med. 21, 62-70
27. Sneddon, J.B., Zhen, H.H., Montgomery, K., Rijn, M., van de, Tward, A.D., West, R., Gladstone, H., Chang, H.Y., Morganroth, G.S., Oro, A.E. et al. (2006) Bone morphogenetic protein antagonist gremlin 1 is widely expressed by cancer-associated stromal cells and can promote tumor cell proliferation. Proc. Natl. Acad. Sci. U.S.A. 103, 14842-14847
28. Veverka, V., Henry, A.J., Slocombe, P.M., Ventom, A., Mulloy, B., Muskett, F.W., Muzylak, M., Greenslade, K., Moore, A., Zhang, L. et al. (2009) Characterization of the structural features and interactions of sclerostin: molecular insight into a key regulator of Wnt-mediated bone formation. J. Biol. Chem. 284, 10890-10900
29. Weidauer, S.E., Schmieder, P., Beerbaum, M., Schmitz, W., Oschkinat, H. and Mueller, T.D. (2009) NMR structure of the Wnt modulator protein Sclerostin. Biochem. Biophys. Res. Commun. 380, 160-165
30. Nolan, K., Kattamuri, C., Luedeke, D.M., Angerman, E.B., Rankin, S.A., Stevens, M.L., Zorn, A.M. and Thompson, T.B. (2015) Structure of neuroblastoma suppressor of tumorigenicity 1 (NBL1): insights for the functional variability across bone morphogenetic protein (BMP) antagonists. J. Biol. Chem. 290, 4759-4771
31. Nolan, K., Kattamuri, C., Luedeke, D.M., Deng, X., Jagpal, A., Zhang, F., Linhardt, R.J., Kenny, A.P., Zorn, A.M. and Thompson, T.B. (2013) Structure of protein related to Dan and Cerberus: insights into the mechanism of bone morphogenetic protein antagonism. Structure 21, 1417-1429
32. Sharma, A., Meyer, F., Hyvonen, M., Best, S.M., Cameron, R.E. and Rushton, N. (2012) Osteoinduction by combining bone morphogenetic protein (BMP)-2 with a bioactive novel nanocomposite. Bone Joint Res. 1, 145-151
33. Zhang, J.-L., Qiu, L.-Y., Kotzsch, A., Weidauer, S., Patterson, L., Hammerschmidt, M., Sebald, W. and Mueller, T.D. (2008) Crystal structure analysis reveals how the Chordin family member crossveinless 2 blocks BMP-2 receptor binding. Dev. Cell 14, 739-750
34. Peränen, J., Rikkonen, M., Hyvönen, M. and Kääriäinen, L. (1996) T7 vectors with modified T7lac promoter for expression of proteins in Escherichia coli. Anal. Biochem. 236, 371-373
35. Brinkmann, U., Mattes, R.E. and Buckel, P. (1989) High-level expression of recombinant genes in Escherichia coli is dependent on the availability of the dnaY gene product. Gene 85, 109-114
36. Katagiri, T., Yamaguchi, A., Komaki, M., Abe, E., Takahashi, N., Ikeda, T., Rosen, V., Wozney, J.M., Fujisawa-Sehara, A. and Suda, T. (1994) Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J. Cell. Biol. 127, 1755-1766
37. Vonrhein, C., Flensburg, C., Keller, P., Sharff, A., Smart, O., Paciorek, W., Womack, T. and Bricogne, G. (2011) Data processing and analysis with the autoPROC toolbox. Acta Crystallogr. D Biol. Crystallogr. 67, 293-302
38. 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
39. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
40. Petoukhov, M.V., Franke, D., Shkumatov, A.V., Tria, G., Kikhney, A.G., Gajda, M., Gorba, C., Mertens, H.D.T., Konarev, P.V. and Svergun, D.I. (2012) New developments in the ATSAS program package for small-angle scattering data analysis. J. Appl. Crystallogr. 45, 342-350
41. Schuck, P. (2004) A model for sedimentation in inhomogeneous media. I. Dynamic density gradients from sedimenting co-solutes. Biophys. Chem. 108, 187-200
42. Church, R.H., Krishnakumar, A., Urbanek, A., Geschwindner, S., Meneely, J., Bianchi, A., Basta, B., Monaghan, S., Elliott, C., Stromstedt, M. et al. (2015) Gremlin1 preferentially binds to bone morphogenetic protein-2 (BMP-2) and BMP-4 over BMP-7. Biochem. J. 466, 55-68
43. Binnerts, M.E., Wen, X., Canté-Barrett, K., Bright, J., Chen, H.-T., Asundi, V., Sattari, P., Tang, T., Boyle, B., Funk, W. et al. (2004) Human Crossveinless-2 is a novel inhibitor of bone morphogenetic proteins. Biochem. Biophys. Res. Commun. 315, 272-280
44. Nakamura, K., Shirai, T., Morishita, S., Uchida, S., Saeki-Miura, K. and Makishima, F. (1999) p38 mitogen-activated protein kinase functionally contributes to chondrogenesis induced by growth/differentiation factor-5 in ATDC5 cells. Exp. Cell Res. 250, 351-363
45. Chiodelli, P., Mitola, S., Ravelli, C., Oreste, P., Rusnati, M. and Presta, M. (2011) Heparan sulfate proteoglycans mediate the angiogenic activity of the vascular endothelial growth factor receptor-2 agonist gremlin. Arterioscler. Thromb. Vasc. Biol. 31, e116-e127
46. Tatsinkam, A.J., Mulloy, B. and Rider, C.C. (2015) Mapping the heparin-binding site of the BMP antagonist gremlin by site-directed mutagenesis based on predictive modelling. Biochem. J. 470, 53-64
47. Laskowski, R.A. and Swindells, M.B. (2011) LigPlot + : multiple ligand-protein interaction diagrams for drug discovery. J. Chem. Inf. Model. 51, 2778-2786
48. Ruppert, R., Hoffmann, E. and Sebald, W. (1996) Human bone morphogenetic protein 2 contains a heparin-binding site which modifies its biological activity. Eur. J. Biochem. 237, 295-302
49. Harrington, A.E., Morris-Triggs, S.A., Ruotolo, B.T., Robinson, C.V., Ohnuma, S.-I. and Hyvönen, M. (2006) Structural basis for the inhibition of activin signalling by follistatin. EMBO J. 25, 1035-1045
50. Lerch, T.F., Shimasaki, S., Woodruff, T.K. and Jardetzky, T.S. (2007) Structural and biophysical coupling of heparin and activin binding to follistatin isoform functions. J. Biol. Chem. 282, 15930-15939
51. Healey, E.G., Bishop, B., Elegheert, J., Bell, C.H., Padilla-Parra, S. and Siebold, C. (2015) Repulsive guidance molecule is a structural bridge between neogenin and bone morphogenetic protein. Nat. Struct. Mol. Biol. 22, 458-465