The structure of the follistatin: Activin complex reveals antagonism of both type I and type II receptor binding

Developmental Cell

Volumn 9, Issue 4, 2005, Pages 535-543

  Thompson, Thomas B ^a,b   Lerch, Thomas F ^a   Cook, Robert W ^a   Woodruff, Teresa K ^a   Jardetzky, Theodore S ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN A; ACTIVIN RECEPTOR 1; ACTIVIN RECEPTOR 2; FOLLISTATIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; CELL DIFFERENTIATION; CELL GROWTH; CRYSTAL STRUCTURE; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN STRUCTURE; RECEPTOR AFFINITY; RECEPTOR BINDING; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; STOICHIOMETRY; STRUCTURE ANALYSIS;

ACTIVIN RECEPTORS, TYPE I; ACTIVINS; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CRICETINAE; CRYSTALLOGRAPHY, X-RAY; FOLLISTATIN; INHIBIN-BETA SUBUNITS; LIGANDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; SEQUENCE ALIGNMENT; TRANSFORMING GROWTH FACTOR BETA;

EID: 26444515002     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2005.09.008     Document Type: Article

References (52)

1. Y. Abe T. Minegishi and P.C. Leung Activin receptor signaling Growth Factors 22 2004 105-110
2. H. Amthor B. Christ F. Rashid-Doubell C.F. Kemp E. Lang and K. Patel Follistatin regulates bone morphogenetic protein-7 (BMP-7) activity to stimulate embryonic muscle growth Dev. Biol. 243 2002 115-127
3. H. Amthor G. Nicholas I. McKinnell C.F. Kemp M. Sharma R. Kambadur and K. Patel Follistatin complexes Myostatin and antagonises Myostatin-mediated inhibition of myogenesis Dev. Biol. 270 2004 19-30
4. A. Aono M. Hazama K. Notoya S. Taketomi H. Yamasaki R. Tsukuda S. Sasaki and Y. Fujisawa Potent ectopic bone-inducing activity of bone morphogenetic protein-4/7 heterodimer Biochem. Biophys. Res. Commun. 210 1995 670-677
5. G.M. Beattie A.D. Lopez N. Bucay A. Hinton M.T. Firpo C.C. King and A. Hayek Activin A maintains pluripotency of human embryonic stem cells in the absence of feeder layers Stem Cells 23 2005 489-495
6. L.M. Bilezikjian A.L. Blount A.M. Leal C.J. Donaldson W.H. Fischer and W.W. Vale Autocrine/paracrine regulation of pituitary function by activin, inhibin and follistatin Mol. Cell. Endocrinol. 225 2004 29-36
7. C. Boileau G. Jondeau T. Mizuguchi and N. Matsumoto Molecular genetics of Marfan syndrome Curr. Opin. Cardiol. 20 2005 194-200
8. A.T. Brunger P.D. Adams G.M. Clore W.L. DeLano P. Gros R.W. Grosse-Kunstleve J.S. Jiang J. Kuszewski M. Nilges and N.S. Pannu Crystallography & NMR system: A new software suite for macromolecular structure determination Acta Crystallogr. D 54 1998 905-921
9. E. Canalis A.N. Economides and E. Gazzerro Bone morphogenetic proteins, their antagonists, and the skeleton Endocr. Rev. 24 2003 218-235
10. H. Chang C.W. Brown and M.M. Matzuk Genetic analysis of the mammalian transforming growth factor-beta superfamily Endocr. Rev. 23 2002 787-823
11. E. de La Fortelle and G. Bricogne Maximum-likelihood heavy-atom parameter refinement in the MIR and MAD methods R.M. Sweet and C.W. Carter eds. In Methods in Enzymology, Macromolecular Crystallography 1997 (Academic Press New York) 472-494
12. S. Dennler M.J. Goumans and P. ten Dijke Transforming growth factor beta signal transduction J. Leukoc. Biol. 71 2002 731-740
13. J.P. deWinter P. ten Dijke C.J.M. de Vries T.A.E. van Achterberg H. Sugino P. de Waele D. Huylebroeck K. Verschueren and A.J.M. van den Eijnden-van Raaij Follistatins neutralize activin bioactivity by inhibition of activin binding to its type II receptors Mol. Cell. Endocrinol. 116 1996 105-114
14. W.H. Fischer M. Park C. Donaldson E. Wiater J. Vaughan L.M. Bilezikjian and W. Vale Residues in the C-terminal region of activin A determine specificity for follistatin and type II receptor binding J. Endocrinol. 176 2003 61-68
15. C. Glister C.F. Kemp and P.G. Knight Bone morphogenetic protein (BMP) ligands and receptors in bovine ovarian follicle cells: Actions of BMP-4, -6 and -7 on granulosa cells and differential modulation of Smad-1 phosphorylation by follistatin Reproduction 127 2004 239-254
16. J. Greenwald J. Groppe P. Gray E. Wiater W. Kwiatkowski W. Vale and S. Choe The BMP7/ActRII extracellular domain complex provides new insights into the cooperative nature of receptor assembly Mol. Cell 11 2003 605-617
17. J. Greenwald M.E. Vega G.P. Allendorph W.H. Fischer W. Vale and S. Choe A flexible activin explains the membrane-dependent cooperative assembly of TGF-beta family receptors Mol. Cell 15 2004 485-489
18. J. Groppe J. Greenwald E. Wiater J. Rodriguez-Leon A.N. Economides W. Kwiatkowski M. Affolter W.W. Vale J.C. Belmonte and S. Choe Structural basis of BMP signalling inhibition by the cystine knot protein Noggin Nature 420 2002 636-642
19. T.L. Gumienny and R.W. Padgett The other side of TGF-beta superfamily signal regulation: Thinking outside the cell Trends Endocrinol. Metab. 13 2002 295-299
20. R. Harland and J. Gerhart Formation and function of Spemann's organizer Annu. Rev. Cell Dev. Biol. 13 1997 611-667
21. C.A. Harrison P.C. Gray W.H. Fischer C. Donaldson S. Choe and W. Vale An activin mutant with disrupted ALK4 binding blocks signaling via type II receptors J. Biol. Chem. 279 2004 28036-28044
22. O. Hashimoto N. Kawasaki K. Tsuchida S. Shimasaki T. Hayakawa and H. Sugino Difference between follistatin isoforms in the inhibition of activin signalling: Activin neutralizing activity of follistatin isoforms is dependent on their affinity for activin Cell. Signal. 12 2000 565-571
23. S. Iemura T.S. Yamamoto C. Takagi H. Uchiyama T. Natsume S. Shimasaki H. Sugino and N. Ueno 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
24. C.A. Innis and M. Hyvonen Crystal structures of the heparan sulfate-binding domain of follistatin. Insights into ligand binding J. Biol. Chem. 278 2003 39969-39977
25. D.I. Israel J. Nove K.M. Kerns R.J. Kaufman V. Rosen K.A. Cox and J.M. Wozney Heterodimeric bone morphogenetic proteins show enhanced activity in vitro and in vivo Growth Factors 13 1996 291-300
26. D. James A.J. Levine D. Besser and A. Hemmati-Brivanlou TGFbeta/activin/ nodal signaling is necessary for the maintenance of pluripotency in human embryonic stem cells Development 132 2005 1273-1282
27. V.G. Kaklamani and B. Pasche Role of TGF-beta in cancer and the potential for therapy and prevention Expert Rev. Anticancer Ther. 4 2004 649-661
28. H.T. Keutmann A.L. Schneyer and Y. Sidis The role of follistatin domains in follistatin biological action Mol. Endocrinol. 18 2004 228-240
29. M.K. Khokha J. Yeh T.C. Grammer and R.M. Harland Depletion of three BMP antagonists from Spemann's organizer leads to a catastrophic loss of dorsal structures Dev. Cell 8 2005 401-411
30. T. Kirsch W. Sebald and M.K. Dreyer Crystal structure of the BMP-2-BRIA ectodomain complex Nat. Struct. Biol. 7 2000 492-496
31. J. Lack J.M. O'Leary V. Knott X. Yuan D.B. Rifkin P.A. Handford and A.K. Downing Solution structure of the third TB domain from LTBP1 provides insight into assembly of the large latent complex that sequesters latent TGF-beta J. Mol. Biol. 334 2003 281-291
32. S.S. Lee V. Knott J. Jovanovic K. Harlos J.M. Grimes L. Choulier H.J. Mardon D.I. Stuart and P.A. Handford Structure of the integrin binding fragment from fibrillin-1 gives new insights into microfibril organization Structure 12 2004 717-729
33. S.Y. Lin J.R. Morrison D.J. Phillips and D.M. de Kretser Regulation of ovarian function by the TGF-beta superfamily and follistatin Reproduction 126 2003 133-148
34. M.M. Matzuk N. Lu H. Vogel K. Sellheyer D.R. Roop and A. Bradley Multiple defects and perinatal death in mice deficient in follistatin Nature 374 1995 360-363
35. S. Nishimatsu and G.H. Thomsen Ventral mesoderm induction and patterning by bone morphogenetic protein heterodimers in Xenopus embryos Mech. Dev. 74 1998 75-88
36. F. Otsuka R.K. Moore S. Iemura N. Ueno and S. Shimasaki Follistatin inhibits the function of the oocyte-derived factor BMP-15 Biochem. Biophys. Res. Commun. 289 2001 961-966
37. S.A. Pangas and T.K. Woodruff Activin signal transduction pathways Trends Endocrinol. Metab. 11 2000 309-314
38. D.B. Rifkin Latent transforming growth factor-beta (TGF-beta) binding proteins: Orchestrators of TGF-beta availability J. Biol. Chem. 280 2005 7409-7412
39. T. Sasaki E. Hohenester W. Gohring and R. Timpl Crystal structure and mapping by site-directed mutagenesis of the collagen-binding epitope of an activated form of BM-40/SPARC/osteonectin EMBO J. 17 1998 1625-1634
40. A. Schneyer A. Schoen A. Quigg and Y. Sidis Differential binding and neutralization of activins A and B by follistatin and follistatin like-3 (FSTL-3/FSRP/FLRG) Endocrinology 144 2003 1671-1674
41. A.L. Schneyer Q. Wang Y. Sidis and P.M. Sluss Differential distribution of follistatin isoforms: Application of a new FS315-specific immunoassay J. Clin. Endocrinol. Metab. 89 2004 5067-5075
42. W. Sebald J. Nickel J.L. Zhang and T.D. Mueller Molecular recognition in bone morphogenetic protein (BMP)/receptor interaction Biol. Chem. 385 2004 697-710
43. Y. Shi and J. Massague Mechanisms of TGF-beta signaling from cell membrane to the nucleus Cell 113 2003 685-700
44. O. Shimmi D. Umulis H. Othmer and M.B. O'Connor Facilitated transport of a Dpp/Scw heterodimer by Sog/Tsg leads to robust patterning of the Drosophila blastoderm embryo Cell 120 2005 873-886
45. P.M. Siegel and J. Massague Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer Nat. Rev. Cancer 3 2003 807-821
46. P.D. Sun and D.R. Davies The cystine-knot growth-factor superfamily Annu. Rev. Biophys. Biomol. Struct. 24 1995 269-291
47. A. Suzuki E. Kaneko J. Maeda and N. Ueno Mesoderm induction by BMP-4 and -7 heterodimers Biochem. Biophys. Res. Commun. 232 1997 153-156
48. T.C. Terwilliger and J. Berendzen Automated MAD and MIR structure solution Acta Crystallogr. D Biol. Crystallogr. 55 1999 849-861
49. T.B. Thompson T.K. Woodruff and T.S. Jardetzky Structures of an ActRIIB: activin A complex reveal a novel binding mode for TGF-beta ligand: receptor interactions EMBO J. 22 2003 1555-1566
50. K. Tsuchida Activins, myostatin and related TGF-beta family members as novel therapeutic targets for endocrine, metabolic and immune disorders Curr. Drug Targets Immune Endocr. Metabol. Disord. 4 2004 157-166
51. Y. Yamamoto and M. Oelgeschlager Regulation of bone morphogenetic proteins in early embryonic development Naturwissenschaften 91 2004 519-534
52. X. Yuan A.K. Downing V. Knott and P.A. Handford Solution structure of the transforming growth factor beta-binding protein-like module, a domain associated with matrix fibrils EMBO J. 16 1997 6659-6666