Crystal Structure Analysis Reveals How the Chordin Family Member Crossveinless 2 Blocks BMP-2 Receptor Binding

Developmental Cell

Volumn 14, Issue 5, 2008, Pages 739-750

  Zhang, Jin li ^a   Qiu, Li yan ^a   Kotzsch, Alexander ^a,b   Weidauer, Stella ^a,b   Patterson, Lucy ^c   Hammerschmidt, Matthias ^c   Sebald, Walter ^a,d   Mueller, Thomas D ^a,b,d  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^d UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

PROTEINS; SIGNALING

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN RECEPTOR 2; CHORDIN; CROSSVEINLESS 2 PROTEIN; VON WILLEBRAND FACTOR;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; CRYSTAL STRUCTURE; EMBRYO; IN VIVO STUDY; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RECEPTOR BINDING; RECEPTOR BLOCKING; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE II; BONE MORPHOGENETIC PROTEINS; CELL LINE; COLLAGEN TYPE II; CRYSTALLOGRAPHY, X-RAY; EPITOPES; FIBRONECTINS; GTPASE-ACTIVATING PROTEINS; HYDROGEN BONDING; HYDROPHOBICITY; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; STRUCTURAL HOMOLOGY, PROTEIN; TRANSFORMING GROWTH FACTOR BETA; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 43049116191     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2008.02.017     Document Type: Article

References (36)

1. Abreu J.G., Ketpura N.I., Reversade B., and De Robertis E.M. Connective-tissue growth factor (CTGF) modulates cell signalling by BMP and TGF-β. Nat. Cell Biol. 4 (2002) 599-604
2. Binnerts M.E., Wen X., Cante-Barrett K., Bright J., Chen H.T., Asundi V., Sattari P., Tang T., Boyle B., Funk W., et al. Human Crossveinless-2 is a novel inhibitor of bone morphogenetic proteins. Biochem. Biophys. Res. Commun. 315 (2004) 272-280
3. Canalis E., Economides A.N., and Gazzerro E. Bone morphogenetic proteins, their antagonists, and the skeleton. Endocr. Rev. 24 (2003) 218-235
4. Coffinier C., Ketpura N., Tran U., Geissert D., and De Robertis E.M. Mouse Crossveinless-2 is the vertebrate homolog of a Drosophila extracellular regulator of BMP signaling. Gene Expr. Patterns 2 (2002) 189-194
5. Coles E., Christiansen J., Economou A., Bronner-Fraser M., and Wilkinson D.G. A vertebrate crossveinless 2 homologue modulates BMP activity and neural crest cell migration. Development 131 (2004) 5309-5317
6. Conley C.A., Silburn R., Singer M.A., Ralston A., Rohwer-Nutter D., Olson D.J., Gelbart W., and Blair S.S. Crossveinless 2 contains cysteine-rich domains and is required for high levels of BMP-like activity during the formation of the cross veins in Drosophila. Development 127 (2000) 3947-3959
7. De Robertis E.M. Spemann's organizer and self-regulation in amphibian embryos. Nat. Rev. Mol. Cell Biol. 7 (2006) 296-302
8. De Robertis E.M., and Kuroda H. Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu. Rev. Cell Dev. Biol. 20 (2004) 285-308
9. Garcia Abreu J., Coffinier C., Larrain J., Oelgeschlager M., and De Robertis E.M. Chordin-like CR domains and the regulation of evolutionarily conserved extracellular signaling systems. Gene 287 (2002) 39-47
10. Groppe J., Greenwald J., Wiater E., Rodriguez-Leon J., Economides A.N., Kwiatkowski W., Affolter M., Vale W.W., Belmonte J.C., and Choe S. Structural basis of BMP signalling inhibition by the cystine knot protein Noggin. Nature 420 (2002) 636-642
11. Hammerschmidt M., Blader P., and Strahle U. Strategies to perturb zebrafish development. Methods Cell Biol. 59 (1999) 87-115
12. Harrington A.E., Morris-Triggs S.A., Ruotolo B.T., Robinson C.V., Ohnuma S., and Hyvonen M. Structural basis for the inhibition of activin signalling by follistatin. EMBO J. 25 (2006) 1035-1045
13. Hatta T., Konishi H., Katoh E., Natsume T., Ueno N., Kobayashi Y., and Yamazaki T. Identification of the ligand-binding site of the BMP type IA receptor for BMP-4. Biopolymers 55 (2000) 399-406
14. Heldin C.H., Miyazono K., and ten Dijke P. TGF-β signalling from cell membrane to nucleus through SMAD proteins. Nature 390 (1997) 465-471
15. Hogan B.L. Bmps: multifunctional regulators of mammalian embryonic development. Harvey Lect. 92 (1996) 83-98
16. Iemura S., Yamamoto T.S., Takagi C., Uchiyama H., Natsume T., Shimasaki S., Sugino H., and Ueno N. Direct binding of follistatin to a complex of bone-morphogenetic protein and its receptor inhibits ventral and epidermal cell fates in early Xenopus embryo. Proc. Natl. Acad. Sci. USA 95 (1998) 9337-9342
17. Ikeya M., Kawada M., Kiyonari H., Sasai N., Nakao K., Furuta Y., and Sasai Y. Essential pro-Bmp roles of crossveinless 2 in mouse organogenesis. Development 133 (2006) 4463-4473
18. Kamimura M., Matsumoto K., Koshiba-Takeuchi K., and Ogura T. Vertebrate crossveinless 2 is secreted and acts as an extracellular modulator of the BMP signaling cascade. Dev. Dyn. 230 (2004) 434-445
19. Keller S., Nickel J., Zhang J.L., Sebald W., and Mueller T.D. Molecular recognition of BMP-2 and BMP receptor IA. Nat. Struct. Mol. Biol. 11 (2004) 481-488
20. Kirsch T., Nickel J., and Sebald W. BMP-2 antagonists emerge from alterations in the low-affinity binding epitope for receptor BMPR-II. EMBO J. 19 (2000) 3314-3324
21. Kirsch T., Sebald W., and Dreyer M.K. Crystal structure of the BMP-2-BRIA ectodomain complex. Nat. Struct. Biol. 7 (2000) 492-496
22. Larrain J., Bachiller D., Lu B., Agius E., Piccolo S., and De Robertis E.M. BMP-binding modules in chordin: a model for signalling regulation in the extracellular space. Development 127 (2000) 821-830
23. Mangino M., Flex E., Digilio M.C., Giannotti A., and Dallapiccola B. Identification of a novel NOG gene mutation (P35S) in an Italian family with symphalangism. Hum. Mutat. 19 (2002) 308
24. Miyazono K., Kusanagi K., and Inoue H. Divergence and convergence of TGF-β/BMP signaling. J. Cell. Physiol. 187 (2001) 265-276
25. Moser M., Binder O., Wu Y., Aitsebaomo J., Ren R., Bode C., Bautch V.L., Conlon F.L., and Patterson C. BMPER, a novel endothelial cell precursor-derived protein, antagonizes bone morphogenetic protein signaling and endothelial cell differentiation. Mol. Cell. Biol. 23 (2003) 5664-5679
26. O'Connor M.B., Umulis D., Othmer H.G., and Blair S.S. Shaping BMP morphogen gradients in the Drosophila embryo and pupal wing. Development 133 (2006) 183-193
27. Oelgeschlager M., Reversade B., Larrain J., Little S., Mullins M.C., and De Robertis E.M. The pro-BMP activity of Twisted gastrulation is independent of BMP binding. Development 130 (2003) 4047-4056
28. O'Leary J.M., Hamilton J.M., Deane C.M., Valeyev N.V., Sandell L.J., and Downing A.K. Solution structure and dynamics of a prototypical chordin-like cysteine-rich repeat (von Willebrand Factor type C module) from collagen IIA. J. Biol. Chem. 279 (2004) 53857-53866
29. Rentzsch F., Zhang J., Kramer C., Sebald W., and Hammerschmidt M. Crossveinless 2 is an essential positive feedback regulator of Bmp signaling during zebrafish gastrulation. Development 133 (2006) 801-811
30. Schier A.F., and Talbot W.S. Molecular genetics of axis formation in zebrafish. Annu. Rev. Genet. 39 (2005) 561-613
31. Tabata T., and Takei Y. Morphogens, their identification and regulation. Development 131 (2004) 703-712
32. Thompson T.B., Lerch T.F., Cook R.W., Woodruff T.K., and Jardetzky T.S. The structure of the follistatin:activin complex reveals antagonism of both type I and type II receptor binding. Dev. Cell 9 (2005) 535-543
33. Weber D., Kotzsch A., Nickel J., Harth S., Seher A., Mueller U., Sebald W., and Mueller T.D. A silent H-bond can be mutationally activated for high-affinity interaction of BMP-2 and activin type IIB receptor. BMC Struct. Biol. 7 (2007) 6
34. Williams M.J., Phan I., Harvey T.S., Rostagno A., Gold L.I., and Campbell I.D. Solution structure of a pair of fibronectin type 1 modules with fibrin binding activity. J. Mol. Biol. 235 (1994) 1302-1311
35. Zhang J.L., Huang Y., Qiu L.Y., Nickel J., and Sebald W. von Willebrand factor type C domain-containing proteins regulate bone morphogenetic protein signaling through different recognition mechanisms. J. Biol. Chem. 282 (2007) 20002-20014
36. Zhu Y., Oganesian A., Keene D.R., and Sandell L.J. Type IIA procollagen containing the cysteine-rich amino propeptide is deposited in the extracellular matrix of prechondrogenic tissue and binds to TGF-β1 and BMP-2. J. Cell Biol. 144 (1999) 1069-1080