A large bioactive BMP ligand with distinct signaling properties is produced by alternative proconvertase processing

Science Signaling

Volumn 5, Issue 218, 2012, Pages

  Akiyama, Takuya ^a,c   Marqués, Guillermo ^b   Wharton, Kristi A ^a  

^a BROWN UNIVERSITY   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 5; BONE MORPHOGENETIC PROTEIN 6; FURIN; LIGAND; OSTEOGENIC PROTEIN 1; TRANSFORMING GROWTH FACTOR BETA; BMP15 PROTEIN, HUMAN; BMP4 PROTEIN, HUMAN; BONE MORPHOGENETIC PROTEIN 15; BONE MORPHOGENETIC PROTEIN 4; DROSOPHILA PROTEIN; GBB PROTEIN, DROSOPHILA; ISOPROTEIN; MUELLERIAN INHIBITING FACTOR; PROTEIN PRECURSOR; SERINE PROTEINASE;

ARTICLE; CLEFT LIP PALATE; ENZYME ACTIVITY; HUMAN; MUELLERIAN DUCT; MUTANT; NONHUMAN; PERSISTENT MULLERIAN DUCT SYNDROME; PREMATURE OVARIAN FAILURE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; SYNDROME; TRANSGENICS; VERTEBRATE; ANIMAL; CELL LINE; CLEFT LIP; CLEFT PALATE; CONGENITAL MALFORMATION; DROSOPHILA MELANOGASTER; FEMALE; FORELIMB; GENETICS; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; MUTATION; PHYLOGENY; TRANSGENIC ANIMAL; WESTERN BLOTTING;

VERTEBRATA;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTI-MULLERIAN HORMONE; BLOTTING, WESTERN; BONE MORPHOGENETIC PROTEIN 15; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEINS; CELL LINE; CLEFT LIP; CLEFT PALATE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; HUMANS; LIGANDS; MALE; MULLERIAN DUCTS; MUTATION; PHYLOGENY; PROPROTEIN CONVERTASES; PROTEIN ISOFORMS; PROTEIN PRECURSORS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; WING;

EID: 84859509735     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2002549     Document Type: Article

References (76)

1. R. Derynck, R. J. Akhurst, A. Balmain, TGF-β signaling in tumor suppression and cancer progression. Nat. Genet. 29, 117-129 (2001).
2. J. Massagué, S. W. Blain, R. S. Lo, TGFβ signaling in growth control, cancer, and heritable disorders. Cell 103, 295-309 (2000).
3. M. Y. Wu, C. S. Hill, TGF-β superfamily signaling in embryonic development and homeostasis. Dev. Cell 16, 329-343 (2009).
4. M. Affolter, K. Basler, The Decapentaplegic morphogen gradient: From pattern formation to growth regulation. Nat. Rev. Genet. 8, 663-674 (2007).
5. E. Bangi, K. Wharton, Dpp and Gbb exhibit different effective ranges in the establishment of the BMP activity gradient critical for Drosophila wing patterning. Dev. Biol. 295, 178-193 (2006).
6. D. A. Dansereau, P. Lasko, The development of germline stem cells in Drosophila. Methods Mol. Biol. 450, 3-26 (2008).
7. B. Bragdon, O. Moseychuk, S. Saldanha, D. King, J. Julian, A. Nohe, Bone morphogenetic proteins: A critical review. Cell. Signal. 23, 609-620 (2011).
8. J. Massagué, The transforming growth factor-b family. Annu. Rev. Cell Biol. 6, 597-641 (1990).
9. Y. Cui, R. Hackenmiller, L. Berg, F. Jean, T. Nakayama, G. Thomas, J. L. Christian, The activity and signaling range of mature BMP-4 is regulated by sequential cleavage at two sites within the prodomain of the precursor. Genes Dev. 15, 2797-2802 (2001).
10. S. Sopory, S. M. Nelsen, C. Degnin, C. Wong, J. L. Christian, Regulation of bone morphogenetic protein-4 activity by sequence elements within the prodomain. J. Biol. Chem. 281, 34021-34031 (2006).
11. D. C. Goldman, R. Hackenmiller, T. Nakayama, S. Sopory, C. Wong, H. Kulessa, J. L. Christian, Mutation of an upstream cleavage site in the BMP4 prodomain leads to tissue-specific loss of activity. Development 133, 1933-1942 (2006).
12. J. Künnapuu, I. Björkgren, O. Shimmi, The Drosophila DPP signal is produced by cleavage of its proprotein at evolutionary diversified furin-recognition sites. Proc. Natl. Acad. Sci. U.S.A. 106, 8501-8506 (2009).
13. S. Sopory, S. Kwon, M. Wehrli, J. L. Christian, Regulation of Dpp activity by tissue-specific cleavage of an upstream site within the prodomain. Dev. Biol. 346, 102-112 (2010).
14. D. B. Constam, E. J. Robertson, Regulation of bone morphogenetic protein activity by pro domains and proprotein convertases. J. Cell Biol. 144, 139-149 (1999).
15. J. Tian, B. Andrée, C. M. Jones, K. Sampath, The pro-domain of the zebrafish Nodal-related protein Cyclops regulates its signaling activities. Development 135, 2649-2658 (2008).
16. Y. Chen, A. F. Schier, The zebrafish Nodal signal Squint functions as a morphogen. Nature 411, 607-610 (2001).
17. T. Akiyama, K. Kamimura, C. Firkus, S. Takeo, O. Shimmi, H. Nakato, Dally regulates Dpp morphogen gradient formation by stabilizing Dpp on the cell surface. Dev. Biol. 313, 408-419 (2008).
18. O. Khalsa, J. W. Yoon, S. Torres-Schumann, K. A. Wharton, TGF-β/BMP superfamily members, Gbb-60A and Dpp, cooperate to provide pattern information and establish cell identity in the Drosophila wing. Development 125, 2723-2734 (1998).
19. R. P. Ray, K. A. Wharton, Context-dependent relationships between the BMPs gbb and dpp during development of the Drosophila wing imaginal disc. Development 128, 3913-3925 (2001).
20. R. K. Blackman, M. Sanicola, L. A. Raftery, T. Gillevet, W. M. Gelbart, An extensive 3′cis-regulatory region directs the imaginal disk expression of decapentaplegic, a member of the TGF-β family in Drosophila. Development 111, 657-666 (1991).
21. A. D. Lander, Q. Nie, F. Y. Wan, Do morphogen gradients arise by diffusion? Dev. Cell 2, 785-796 (2002).
22. A. Kicheva, M. Gonzalez-Gaitan, The Decapentaplegic morphogen gradient: A precise definition. Curr. Opin. Cell Biol. 20, 137-143 (2008).
23. G. Schwank, S. Dalessi, S. F. Yang, R. Yagi, A. M. de Lachapelle, M. Affolter, S. Bergmann, K. Basler, Formation of the long range Dpp morphogen gradient. PLoS Biol. 9, e1001111 (2011).
24. M. P. Schlunegger, M. G. Grutter, An unusual feature revealed by the crystal structure at 2.2 Å resolution of human transforming growth factor-β2. Nature 358, 430-434 (1992).
25. S. Daopin, K. A. Piez, Y. Ogawa, D. R. Davies, Crystal structure of transforming growth factor-β2: An unusual fold for the superfamily. Science 257, 369-373 (1992).
26. S. Imbeaud, D. Carre-Eusebe, R. Rey, C. Belville, N. Josso, J. Y. Picard, Molecular genetics of the persistent Müllerian duct syndrome: A study of 19 families. Hum. Mol. Genet. 3, 125-131 (1994).
27. H. Dixit, L.K. Rao, V. V. Padmalatha, M. Kanakavalli, M. Deenadayal, N. Gupta, B. Chakrabarty, L. Singh, Missense mutations in the BMP15 gene are associated with ovarian failure. Hum. Genet. 119, 408-415 (2006).
28. S. Suzuki, M. L. Marazita, M. E. Cooper, N. Miwa, A. Hing, A. Jugessur, N. Natsume, K. Shimozato, N. Ohbayashi, Y. Suzuki, T. Niimi, K. Minami, M. Yamamoto, T. J. Altannamar, T. Erkhembaatar, H. Furukawa, S. Daack-Hirsch, J. L'Heureux, C. A. Brandon, S. M. Weinberg, K. Neiswanger, F.W. Deleyiannis, J. E. de Salamanca, A. R. Vieira, A. C. Lidral, J. F. Martin, J. C. Murray, Mutations in BMP4 are associated with subepithelial, microform, and overt cleft lip. Am. J. Hum. Genet. 84, 406-411 (2009).
29. B. Müller, B. Hartmann, G. Pyrowolakis, M. Affolter, K. Basler, Conversion of an extracellular Dpp/BMP morphogen gradient into an inverse transcriptional gradient. Cell 113, 221-233 (2003).
30. G. Pyrowolakis, B. Hartmann, B. Müller, K. Basler, M. Affolter, A simple molecular complex mediates widespread BMP-induced repression during Drosophila development. Dev. Cell 7, 229-240 (2004).
31. E. Bangi, K. Wharton, Dual function of the Drosophila Alk1/Alk2 ortholog Saxophone shapes the BMP activity gradient in the wing imaginal disc. Development 133, 3295-3303 (2006).
32. C. Degnin, F. Jean, G. Thomas, J. L. Christian, Cleavages within the prodomain direct intracellular trafficking and degradation of mature bone morphogenetic protein-4. Mol. Biol. Cell 15, 5012-5020 (2004).
33. T. E. Haerry, The interaction between two TGF-β type I receptors plays important roles in ligand binding, SMAD activation, and gradient formation. Mech. Dev. 127, 358-370 (2010).
34. M. Shi, J. Zhu, R. Wang, X. Chen, L. Mi, T. Walz, T. A. Springer, Latent TGF-β structure and activation. Nature 474, 343-349 (2011).
35. A. C. Daly, R. A. Randall, C. S. Hill, Transforming growth factor β-induced Smad1/5 phosphorylation in epithelial cells is mediated by novel receptor complexes and is essential for anchorage-independent growth. Mol. Cell. Biol. 28, 6889-6902 (2008).
36. K. A. Wharton, J. M. Cook, S. Torres-Schumann, K. de Castro, E. Borod, D. A. Phillips, Genetic analysis of the bone morphogenetic protein-related gene, gbb, identifies multiple requirements during Drosophila development. Genetics 152, 629-640 (1999).
37. J. Bischof, R. K. Maeda, M. Hediger, F. Karch, K. Basler, An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. U.S.A. 104, 3312-3317 (2007).
38. A. R. Lopez, J. Cook, P. L. Deininger, R. Derynck, Dominant negative mutants of transforming growth factor-β1 inhibit the secretion of different transforming growth factor-β isoforms. Mol. Cell. Biol. 12, 1674-1679 (1992).
39. J. Wittbrodt, F. M. Rosa, Disruption of mesoderm and axis formation in fish by ectopic expression of activin variants: The role of maternal activin. Genes Dev. 8, 1448-1462 (1994).
40. S. H. Hawley, K. Wunnenberg-Stapleton, C. Hashimoto, M. N. Laurent, T. Watabe, B. W. Blumberg, K.W. Cho, Disruption of BMP signals in embryonic Xenopus ectoderm leads to direct neural induction. Genes Dev. 9, 2923-2935 (1995).
41. S. I. Osada, C. V. Wright, Xenopus nodal-related signaling is essential for mesendodermal patterning during early embryogenesis. Development 126, 3229-3240 (1999).
42. B. I. Sun, S. M. Bush, L. A. Collins-Racie, E. R. LaVallie, E. A. DiBlasio-Smith, N. M. Wolfman, J. M. McCoy, H. L. Sive, derrière: A TGF-β family member required for posterior development in Xenopus. Development 126, 1467-1482 (1999).
43. E. M. Joseph, D. A. Melton, Mutant Vg1 ligands disrupt endoderm and mesoderm formation in Xenopus embryos. Development 125, 2677-2685 (1998).
44. P. M. Eimon, R. M. Harland, Effects of heterodimerization and proteolytic processing on Derrière and Nodal activity: Implications for mesoderm induction in Xenopus. Development 129, 3089-3103 (2002).
45. W. M. Gelbart, The decapentaplegic gene: A TGF-β homologue controlling pattern formation in Drosophila. Development 107 (Suppl.), 65-74 (1989).
46. Y. Tomoyasu, M. Nakamura, N. Ueno, Role of dpp signalling in prepattern formation of the dorsocentral mechanosensory organ in Drosophila melanogaster. Development 125, 4215-4224 (1998).
47. H. Tanimoto, S. Itoh, P. ten Dijke, T. Tabata, Hedgehog creates a gradient of DPP activity in Drosophila wing imaginal discs. Mol. Cell 5, 59-71 (2000).
48. O. Wartlick, P. Mumcu, A. Kicheva, T. Bittig, C. Seum, F. Julicher, M. Gonzalez-Gaitan, Dynamics of Dpp signaling and proliferation control. Science 331, 1154-1159 (2011).
49. F. Hamaratoglu, A. M. de Lachapelle, G. Pyrowolakis, S. Bergmann, M. Affolter, Dpp signaling activity requires Pentagone to scale with tissue size in the growing Drosophila wing imaginal disc. PLoS Biol. 9, e1001182 (2011).
50. M. Fujise, S. Takeo, K. Kamimura, T. Matsuo, T. Aigaki, S. Izumi, H. Nakato, Dally regulates Dpp morphogen gradient formation in the Drosophila wing. Development 130, 1515-1522 (2003).
51. K. Dejima, M. I. Kanai, T. Akiyama, D. C. Levings, H. Nakato, Novel contact-dependent bone morphogenetic protein (BMP) signaling mediated by heparan sulfate proteoglycans. J. Biol. Chem. 286, 17103-17111 (2011).
52. S. J. Lee, A. C. McPherron, Regulation of myostatin activity and muscle growth. Proc. Natl. Acad. Sci. U.S.A. 98, 9306-9311 (2001).
53. M. S. Jiang, L. F. Liang, S. Wang, T. Ratovitski, J. Holmstrom, C. Barker, R. Stotish, Characterization and identification of the inhibitory domain of GDF-8 propeptide. Biochem. Biophys. Res. Commun. 315, 525-531 (2004).
54. J. Varga, B. Pasche, Antitransforming growth factor-β therapy in fibrosis: Recent progress and implications for systemic sclerosis. Curr. Opin. Rheumatol. 20, 720-728 (2008).
55. A. Hauburger, S. von Einem, G. K. Schwaerzer, A. Buttstedt, M. Zebisch, M. Schraml, P. Hortschansky, P. Knaus, E. Schwarz, The pro-form of BMP-2 interferes with BMP-2 signalling by competing with BMP-2 for IA receptor binding. FEBS J. 276, 6386-6398 (2009).
56. G. Sengle, R. N. Ono, K. M. Lyons, H. P. Bachinger, L. Y. Sakai, A new model for growth factor activation: Type II receptors compete with the prodomain for BMP-7. J. Mol. Biol. 381, 1025-1039 (2008).
57. N. di Clemente, S. P. Jamin, A. Lugovskoy, P. Carmillo, C. Ehrenfels, J. Y. Picard, A. Whitty, N. Josso, R. B. Pepinsky, R. L. Cate, Processing of anti-Müllerian hormone regulates receptor activation by a mechanism distinct from TGF-β. Mol. Endocrinol. 24, 2193-2206 (2010).
58. S. Kuhfahl, A. Hauburger, T. Thieme, J. Groppe, C. Ihling, S. Tomic, M. Schutkowski, A. Sinz, E. Schwarz, Identification of a core domain within the proregion of bone morphogenetic proteins that interacts with the dimeric, mature domain. Biochem. Biophys. Res. Commun. 408, 300-305 (2011).
59. Y. Ogiso, K. Tsuneizumi, N. Masuda, M. Sato, T. Tabata, Robustness of the Dpp morphogen activity gradient depends on negative feedback regulation by the inhibitory Smad, Dad. Dev. Growth Differ. 53, 668-678 (2011).
60. W. Liu, X. Sun, A. Braut, Y. Mishina, R. R. Behringer, M. Mina, J. F. Martin, Distinct functions for Bmp signaling in lip and palate fusion in mice. Development 132, 1453-1461 (2005).
61. B. L. M. Hogan, Bone morphogenetic proteins: Multifunctional regulators of vertebrate development. Genes Dev. 10, 1580-1594 (1996).
62. R. Derynck, K. Miyazono, Eds., The TGF-β Family (Cold Spring Harbor Laboratory Press, New York, 2008), vol. 50.
63. P. Wu, T. X. Jiang, S. Suksaweang, R. B. Widelitz, C. M. Chuong, Molecular shaping of the beak. Science 305, 1465-1466 (2004).
64. A. Abzhanov, M. Protas, B. R. Grant, P. R. Grant, C. J. Tabin, Bmp4 and morphological variation of beaks in Darwin's finches. Science 305, 1462-1465 (2004).
65. R. C. Albertson, T. D. Kocher, Genetic and developmental basis of cichlid trophic diversity. Heredity 97, 211-221 (2006).
66. Y. Terai, N. Morikawa, N. Okada, The evolution of the pro-domain of bone morphogenetic protein 4 (Bmp4) in an explosively speciated lineage of East African cichlid fishes. Mol. Biol. Evol. 19, 1628-1632 (2002).
67. S. Tweedie, M. Ashburner, K. Falls, P. Leyland, P. McQuilton, S. Marygold, G. Millburn, D. Osumi-Sutherland, A. Schroeder, R. Seal, H. Zhang; Flybase Consortium, FlyBase: Enhancing Drosophila Gene Ontology annotations. Nucleic Acids Res. 37, D555-D559 (2009).
68. K. G. Golic, S. Lindquist, The FLP recombinase of yeast catalyzes site-specific recombination in the Drosophila genome. Cell 59, 499-509 (1989).
69. G. Struhl, K. Basler, Organizing activity of wingless protein in Drosophila. Cell 72, 527-540 (1993).
70. K. A. Wharton, G. H. Thomsen, W. M. Gelbart, Drosophila 60A gene, another transforming growth factor b family member, is closely related to human bone morphogenetic proteins. Proc. Natl. Acad. Sci. U.S.A. 88, 9214-9218 (1991).
71. J. J. Ross, O. Shimmi, P. Vilmos, A. Petryk, H. Kim, K. Gaudenz, S. Hermanson, S. C. Ekker, M. B. O'Connor, J. L. Marsh, Twisted gastrulation is a conserved extracellular BMP antagonist. Nature 410, 479-483 (2001).
72. M. Nahm, A. A. Long, S. K. Paik, S. Kim, Y. C. Bae, K. Broadie, S. Lee, The Cdc42-selective GAP rich regulates postsynaptic development and retrograde BMP transsynaptic signaling. J. Cell Biol. 191, 661-675 (2010).
73. O. Korchynskyi, P. ten Dijke, Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J. Biol. Chem. 277, 4883-4891 (2002).
74. L. Zilberberg, P. ten Dijke, L. Y. Sakai, D. B. Rifkin, A rapid and sensitive bioassay to measure bone morphogenetic protein activity. BMC Cell Biol. 8, 41 (2007).
75. R. Barrio, J. F. de Celis, Regulation of spalt expression in the Drosophila wing blade in response to the Decapentaplegic signaling pathway. Proc. Natl. Acad. Sci. U.S.A. 101, 6021-6026 (2004).
76. P. Duckert, S. Brunak, N. Blom, Prediction of proprotein convertase cleavage sites. Protein Eng. Des. Sel. 17, 107-112 (2004).