Enzymatic regulation of pattern: BMP4 binds CUB domains of Tolloids and inhibits proteinase activity

Genes and Development

Volumn 23, Issue 21, 2009, Pages 2551-2562

  Lee, Hojoon X ^a   Mendes, Fabio A ^a   Plouhinec, Jean Louis ^a   De Robertis, Edward M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

BMP; BMP1; Chordin; CUB domain; Tolloid

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; CELL PROTEIN; CHORDIN; METALLOPROTEINASE; PROCOLLAGEN C PROTEINASE; PROTEIN COMPLEMENT 1R S; PROTEIN UEGF; PROTEINASE; TOLLOID DERIVATIVE; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ALLELE; ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DROSOPHILA; EMBRYO; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME INHIBITION; ENZYME REGULATION; FEEDBACK SYSTEM; FLUOROMETRY; MATHEMATICAL MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; XENOPUS;

ANIMALS; BODY PATTERNING; BONE MORPHOGENETIC PROTEIN 1; BONE MORPHOGENETIC PROTEIN 4; COMPLEMENT C1R; COMPLEMENT C1S; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; ENZYME INHIBITORS; FEEDBACK, PHYSIOLOGICAL; PROTEIN STRUCTURE, TERTIARY; TOLLOID-LIKE METALLOPROTEINASES; XENOPUS LAEVIS; XENOPUS PROTEINS;

ECHINOIDEA;

EID: 70350655653     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1839309     Document Type: Article

References (54)

1. Ambrosio AL, Taelman VF, Lee HX, Metzinger CA, Coffinier C, De Robertis EM. 2008. Crossveinless-2 is a BMP feedback inhibitor that binds Chordin/BMP to regulate Xenopus embryonic patterning. Dev Cell 15: 248-260.
2. Ben-Zvi D, Shilo BZ, Fainsod A, Barkai N. 2008. Scaling of the BMP activation gradient in Xenopus embryos. Nature 453: 1205-1211. (Pubitemid 351913602)
3. Blitz IL, Shimmi O, Wünnenberg-Stapleton K, O'Connor MB, Cho KW. 2000. Is chordin a long-range- or short-range-acting factor? Roles for BMP1-related metalloproteases in chordin and BMP4 autofeedback loop regulation Dev Biol 223: 120-138.
4. Bork P, Beckmann G. 1993. The CUB domain. A widespread module in developmentally regulated proteins. J Mol Biol 231: 539-545. (Pubitemid 23188276)
5. Canty EG, Garrigue-Antar L, Kadler KE. 2006. A complete domain structure of Drosophila tolloid is required for cleavage of short gastrulation. J Biol Chem 281: 13258-13267. (Pubitemid 43855237)
6. Celeste AJ, Iannazzi JA, Taylor RC, Hewick RM, Rosen V, Wang EA, Wozney JM. 1990. Identification of transforming growth factor β family members present in bone-inductive protein purified from bovine bone. Proc Natl Acad Sci 87: 9843-9847. (Pubitemid 120016540)
7. Childs S, O'Connor MB. 1994. Two domains of the tolloid protein contribute to its unusual genetic interaction with decapentaplegic. Dev Biol 162: 209-220. (Pubitemid 24098544)
8. Dale L, Evans W, Goodman SA. 2002. Xolloid-related: A novel BMP1/Tolloid-related metalloprotease is expressed during early Xenopus development. Mech Dev 119: 177-190. (Pubitemid 35430106)
9. De Robertis EM. 2008. Evo-Devo: Variations on ancestral themes. Cell 132: 185-195.
10. De Robertis EM, Kuroda H. 2004. Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu Rev Cell Dev Biol 20: 285-308. (Pubitemid 39488640)
11. Dixon M, Webb EC. 1979. Enzymes. Academic, New York.
12. Eldar A, Dorfman R,Weiss D, Ashe H, Shilo BZ, Barkai N. 2002. Robustness of the BMP morphogen gradient in Drosophila embryonic patterning. Nature 419: 304-308.
13. Ferguson EL, Anderson KV. 1992. Localized enhancement and repression of the activity of the TGF-β family member, decapentaplegic, is necessary for dorsal-ventral pattern formation in the Drosophila embryo. Development 114: 583-597.
14. Finelli AL, Bossie CA, Xie T, Padgett RW. 1994. Mutation analysis of the Drosophila tolloid gene, a human BMP-1 homolog. Development 120: 861-870. (Pubitemid 24111551)
15. Geach TJ, Dale L. 2008. Molecular determinants of Xolloid action in vivo. J Biol Chem 283: 27057-27063.
16. Greenspan DS. 2005. Biosynthetic processing of collagen molecules. Top Curr Chem 247: 149-183.
17. Hartigan N, Garrigue-Antar L, Kadler KE. 2003. Bone morphogenetic protein-1 (BMP-1). Identification of the minimal domain structure for procollagen C-proteinase activity. J Biol Chem 278: 18045-18049. (Pubitemid 36799415)
18. Hojima Y, van der Rest M, Prockop DJ. 1985. Type I procollagen carboxyl-terminal proteinase from chick embryo tendons. J Biol Chem 260: 15996-16003.
19. Hopkins DR, Keles S, Greenspan DS. 2007. The bone morphogenetic protein 1/Tolloid-like metalloproteinases. Matrix Biol 26: 508-523. (Pubitemid 47575882)
20. Inomata H, Haraguchi T, Sasai Y. 2008. Robust stability of the embryonic axial pattern requires a secreted scaffold for chordin degradation. Cell 134: 854-865.
21. Jasuja R, Voss N, Ge G, Hoffman GG, Lyman-Gingerich J, Pelegri F, Greenspan DS. 2006. bmp1 and mini fin are functionally redundant in regulating formation of the zebrafish dorosoventral axis. Mech Dev 123: 548-558. (Pubitemid 44176345)
22. Jasuja R, Ge G, Voss NG, Lyman-Gingerich J, Branam AM, Pelegri FJ, Greenspan DS. 2007. Bone morphogenetic protein 1 prodomain specifically binds and regulates signaling by bone morphogenetic proteins 2 and 4. J Biol Chem 282: 9053-9062. (Pubitemid 47093539)
23. Jürgens G, Wieschaus E, Nüsslein-Volhard C, Kluding H. 1984. Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. Rouxs Arch Dev Biol 193: 283-293.
24. Khokha MK, Yeh J, Grammer TC, Harland RM. 2005. Depletion of three BMP antagonists from Spemann's organizer leads to a catastrophic loss of dorsal structures. Dev Cell 8: 401-411. (Pubitemid 40309810)
25. Larraín J, Bachiller D, Lu B, Agius E, Piccolo S, De Robertis EM. 2000. BMP-binding modules in Chordin: A model for signalling regulation in the extracellular space. Development 127: 821-830. (Pubitemid 30129028)
26. Lee HX, Ambrosio AL, Reversade B, De Robertis EM. 2006. Embryonic dorsal-ventral signaling: Secreted Frizzled-related proteins as inhibitors of Tolloid proteinases. Cell 124: 147-159. (Pubitemid 43069316)
27. Levander G. 1938. A study of bone regeneration. Surg Gynecol Obstet 67: 705-714.
28. Little SC, Mullins MC. 2006. Extracellular modulation of BMP activity in patterning the dorsoventral axis. Birth Def Res 78: 224-242.
29. Mao B, Wu W, Davidson G, Marhold J, Li M, Mechler BM, Delius H, Hoppe D, Stannek P,Walter C, et al. 2002. Kremen proteins are Dickkopf receptors that regulate Wnt/β-catenin signalling. Nature 417: 664-667. (Pubitemid 34614827)
30. Marqués G, Musacchio M, Shimell MJ, Wünnenberg-Stapleton K, Cho KWY, O'Connor MB. 1997. Production of DPP activity gradient in the early Drosophila embryo through the opposing actions of the SOG and TLD proteins. Cell 91: 417-426. (Pubitemid 27467972)
31. Meinhardt H, Gierer A. 2000. Pattern formation by local self-activation and lateral inhibition. Bioessays 22: 753-760. (Pubitemid 30613307)
32. Mizutani CM, Nie Q, Wan FY, Zhang YT, Vilmos P, Sousa-Neves R, Bier E, Marsh JL, Lander AD. 2005. Formation of the BMP activity gradient in the Drosophila embryo. Dev Cell 8: 915-924. (Pubitemid 40754062)
33. Muraoka O, Shimizu T, Yabe T, Nojima H, Bae YK, Hashimoto H, Hibi M. 2006. Sizzled controls dorso-ventral polarity by repressing cleavage of the Chordin protein. Nat Cell Biol 8: 329-338.
34. O'Connor MB, Umulis D, Othmer HG, Blair SS. 2006. Shaping BMP morphogens gradients in the Drosophila embryo and pupal wing. Development 133: 183-193. (Pubitemid 43210708)
35. Oelgeschläger M, Kuroda H, Reversade B, De Robertis EM. 2003. Chordin is required for the Spemann organizer transplantation phenomenon in Xenopus embryos. Dev Cell 4: 219-230. (Pubitemid 36221798)
36. Petropoulou V, Garrigue-Antar L, Kadler KE. 2005. Identification of the minimal domain structure of bone morphogenetic protein-1 (BMP-1) for chordinase activity: Chordinase activity is not enhanced by procollagen C-proteinase enhancer-1 (PCPE-1). J Biol Chem 280: 22616-22623. (Pubitemid 40853165)
37. Piccolo S, Agius E, Lu B, Goodman S, Dale L, De Robertis EM. 1997. Cleavage of Chordin by the Xolloid metalloprotease suggests a role for proteolytic processing in the regulation of Spemann organizer activity. Cell 91: 407-416. (Pubitemid 27467971)
38. Piccolo S, Agius E, Leyns L, Battacharyya S, Grunz H, Bouwmeester T, De Robertis EM. 1999. The head inducer Cerberus is a multifunctional antagonist of Nodal, BMP and Wnt signals. Nature 397: 707-710. (Pubitemid 29108391)
39. Plouhinec JL, De Robertis EM. 2009. Systems biology of the self-regulating morphogenetic gradient of the Xenopus gastrula. Cold Spring Harb Perspect Biol 1: a001701. doi: 10.1101/cshperspect.a001701.
40. Reversade B, De Robertis EM. 2005. Regulation of ADMP and BMP2/4/7 at opposite embryonic poles generates a self-regulating morphogen field. Cell 123: 1147-1160. (Pubitemid 41785427)
41. Sampath TK, Reddi AH. 1981. Dissociative extraction and reconstitution of extracellular matrix components involved in local bone differentiation. Proc Natl Acad Sci 78: 7599-7603. (Pubitemid 12186190)
42. Serpe M, Umulis D, Ralston A, Chen J, Olson DJ, Avanesov A, Othmer H, O'Connor MB, Blair SS. 2008. The BMP-binding protein Crossveinless 2 is a short-range, concentration-dependent, biphasic modulator of BMP signaling in Drosophila. Dev Cell 14: 940-953. (Pubitemid 351757202)
43. Shimmi O, Umulis D, Othmer H, O'Connor MB. 2005. Facilitated transport of a Dpp/Scw heterodimer by Sog/Tsg leads to robust patterning of the Drosophila blastoderm embryo. Cell 120: 873-886. (Pubitemid 40568802)
44. Siva AC, Wild MA, Kirkland RE, Nolan MJ, Lin B, Maruyama T, Yantiri F, Fredickson S, Bowdish KS, Xin H. 2008. Targeting CUB domain-containing protein 1 with a monoclonal antibody inhibits metastasis in a prostate cancer model. Cancer Res 68: 3759-3766.
45. Sundin OH, Leppert GS, Silva ED, Yang JM, Dharmaraj S, Maumenee IH, Santos LC, Parsa CF, Traboulsi EI, Broman KW, et al. 2005. Extreme hyperopia is the result of null mutations in MFRP, which encodes a Frizzled-related protein. Proc Natl Acad Sci 102: 9553-9558. (Pubitemid 40981719)
46. Takahara K, Kessler E, Biniaminov L, Brusel M, Eddy RL, Jani-Sait S, Shows TB, Greenspan DS. 1994. Type I procollagen COOH-terminal proteinase enhancer protein: Identification, primary structure, and chromosomal localization of the cognate human gene PCOLCE. J Biol Chem 269: 26280-26285. (Pubitemid 24328445)
47. Turing AM. 1952. The chemical basis of morphogenesis. Philos Trans R Soc Lond 237: 37-72.
48. Tucker JA, Mintzer KA, Mullins MC. 2008. The BMP signaling gradient patterns dorsoventral tissues in a temporally progressive manner along the anteroposterior axis. Dev Cell 14: 108-119.
49. Umulis DM, Serpe M, O'Connor MB, Othmer HG. 2006. Robust, bistable patterning of the dorsal surface of the Drosophila embryo. Proc Natl Acad Sci 103: 11613-11618. (Pubitemid 44182500)
50. Urist M. 1965. Bone: Formation by autoinduction. Science 150: 893-899.
51. Wang YC, Ferguson EL. 2005. Spatial bistability of Dpp-receptor interactions during Drosophila dorsal-ventral patterning. Nature 434: 229-234.
52. Wardle FC, Welch JV, Dale L. 1999. Bone morphogenetic protein 1 regulates dorsal-ventral patterning in early Xenopus embryos by degrading chordin, a BMP4 antagonist. Mech Dev 86: 75-85. (Pubitemid 29371745)
53. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM, Wang EA. 1988. Novel regulators of bone formation: Molecular clones and activities. Science 242: 1528-1534. (Pubitemid 19023695)
54. Zhang JL, Huang Y, Qiu LY, Nickel J, Sebald W. 2007. von Willebrand factor type C domain-containing proteins regulate bone morphogenetic protein signaling through different recognition mechanisms. J Biol Chem 282: 20002-20014. (Pubitemid 47100074)