Bone morphogenetic protein heterodimers assemble heteromeric type I receptor complexes to pattern the dorsoventral axis

Nature Cell Biology

Volumn 11, Issue 5, 2009, Pages 637-643

  Little, Shawn C ^a   Mullins, Mary C ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN LIKE KINASE 3; ACTIVIN LIKE KINASE 6; ACTIVIN LIKE KINASE 8; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; HETERODIMER; HOMODIMER; LIGAND; MESSENGER RNA; OSTEOGENIC PROTEIN 1; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; IMMUNOPRECIPITATION; MOLECULAR CLONING; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; RECEPTOR AFFINITY; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ZEBRA FISH;

ACTIVIN RECEPTORS; ACTIVIN RECEPTORS, TYPE I; ANIMALS; BODY PATTERNING; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 7; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE I; BONE MORPHOGENETIC PROTEINS; CELL NUCLEUS; EMBRYO, NONMAMMALIAN; MODELS, BIOLOGICAL; OLIGONUCLEOTIDES, ANTISENSE; PHOSPHORYLATION; PROTEIN BINDING; RNA, MESSENGER; SIGNAL TRANSDUCTION; SMAD1 PROTEIN; SMAD5 PROTEIN; ZEBRAFISH; ZEBRAFISH PROTEINS;

DANIO RERIO; DROSOPHILA MELANOGASTER; INVERTEBRATA; VERTEBRATA;

EID: 67349187409     PISSN: 14657392     EISSN: None     Source Type: Journal    
DOI: 10.1038/ncb1870     Document Type: Article

References (44)

1. Little, S. C. & Mullins, M. C. Extracellular modulation of BMP activity in patterning the dorsoventral axis. Birth Defects Res. C Embryo Today 78, 224-242 (2006).
2. Shimmi, O., Umulis, D., Othmer, H. & O'Connor, M. B. Facilitated transport of a Dpp/Scw heterodimer by Sog/Tsg leads to robust patterning of the Drosophila blastoderm embryo. Cell 120, 873-886 (2005).
3. Wang, Y. C. & Ferguson, E. L. Spatial bistability of Dpp-receptor interactions during Drosophila dorsal-ventral patterning. Nature 434, 229-234 (2005).
4. Feng, X. H. & Derynck, R. Specificity and versatility in TGF-β signaling through Smads. Annu. Rev. Cell Dev. Biol. 21, 659-693 (2005).
5. O'Connor, M. B., Umulis, D., Othmer, H. G. & Blair, S. S. Shaping BMP morphogen gradients in the Drosophila embryo and pupal wing. Development 133, 183-193 (2006).
6. Kishigami, S. & Mishina, Y. BMP signaling and early embryonic patterning. Cytokine Growth Factor Rev. 16, 265-278 (2005).
7. Schmid, B. et al. Equivalent genetic roles for bmp7/ snailhouse and bmp2b/swirl in dorsoventral pattern formation. Development 127, 957-967 (2000).
8. Yelick, P. C., Abduljabbar, T. S. & Stashenko, P. zALK-8, a novel type I serine/threonine kinase receptor, is expressed throughout early zebrafish development. Dev. Dyn. 211, 352-361 (1998).
9. Nikaido, M., Tada, M., Takeda, H., Kuroiwa, A. & Ueno, N. In vivo analysis using variants of zebrafish BMPR-IA: Range of action and involvement of BMP in ectoderm patterning. Development 126, 181-190 (1999).
10. Nikaido, M., Tada, M. & Ueno, N. Restricted expression of the receptor serine/threonine kinase BMPR-IB in zebrafish. Mech. Dev. 82, 219-222 (1999).
11. Woods, I. G. et al. The zebrafish gene map defines ancestral vertebrate chromosomes. Genome Res. 15, 1307-1314 (2005).
12. Bauer, H., Lele, Z., Rauch, G. J., Geisler, R. & Hammerschmidt, M. The type I serine/threonine kinase receptor Alk8/Lost-a-fin is required for Bmp2b/7 signal transduction during dorsoventral patterning of the zebrafish embryo. Development 128, 849-858 (2001).
13. Mintzer, K. A. et al. Lost-a-fin encodes a type I BMP receptor, Alk8, acting maternally and zygotically in dorsoventral pattern formation. Development 128, 859-869 (2001).
14. Mullins, M. C. et al. Genes establishing dorsoventral pattern formation in the zebrafish embryo: The ventral specifying genes. Development 123, 81-93 (1996).
15. Imai, Y. & Talbot, W. S. Morpholino phenocopies of the bmp2b/swirl and bmp7/snail-house mutations. Genesis 30, 160-163 (2001).
16. Sampath, T. K. et al. Bovine osteogenic protein is composed of dimers of OP-1 and BMP-2A, two members of the transforming growth factor-β superfamily. J. Biol. Chem. 265, 13198-13205 (1990).
17. Cui, Y., Jean, F., Thomas, G. & Christian, J. L. BMP-4 is proteolytically activated by furin and/or PC6 during vertebrate embryonic development. EMBO J. 17, 4735-4743 (1998).
18. Tucker, J. A., Mintzer, K. A. & Mullins, M. C. The BMP signaling gradient patterns dorsoventral tissues in a temporally progressive manner along the anteroposterior axis. Dev. Cell 14, 108-119 (2008).
19. Yeo, C. & Whitman, M. Nodal signals to Smads through Cripto-dependent and Criptoindependent mechanisms. Mol. Cell 7, 949-957 (2001).
20. Gilboa, L., Wells, R. G., Lodish, H. F. & Henis, Y. I. Oligomeric structure of type I and type II transforming growth factor β receptors: homodimers form in the ER and persist at the plasma membrane. J. Cell Biol. 140, 767-777 (1998).
21. Gilboa, L. et al. Bone morphogenetic protein receptor complexes on the surface of live cells: A new oligomerization mode for serine/ threonine kinase receptors. Mol. Biol. Cell 11, 1023-1035 (2000).
22. Graff, J. M., Thies, R. S., Song, J. J., Celeste, A. J. & Melton, D. A. Studies with a Xenopus BMP receptor suggest that ventral mesoderm-inducing signals override dorsal signals in vivo. Cell 79, 169-179 (1994).
23. Koenig, B. B. et al. Characterization and cloning of a receptor for BMP-2 and BMP-4 from NIH 3T3 cells. Mol. Cell. Biol. 14, 5961-5974 (1994).
24. Kirsch, T., Nickel, J. & Sebald, W. BMP-2 antagonists emerge from alterations in the low-affinity binding epitope for receptor BMPR-II. EMBO J. 19, 3314-3324 (2000).
25. Macias-Silva, M., Hoodless, P. A., Tang, S. J., Buchwald, M. & Wrana, J. L. Specific activation of Smad1 signaling pathways by the BMP7 type I receptor, ALK2. J. Biol. Chem. 273, 25628-25636 (1998).
26. Greenwald, J. et al. The BMP7/ActRII extracellular domain complex provides new insights into the cooperative nature of receptor assembly. Mol. Cell 11, 605-617 (2003).
27. Scheufler, C., Sebald, W. & Hulsmeyer, M. Crystal structure of human bone morphogenetic protein-2 at 2.7 A resolution. J. Mol. Biol. 287, 103-115 (1999).
28. Weber, D. et al. A silent H-bond can be mutationally activated for high-affinity interaction of BMP-2 and activin type IIB receptor. BMC Struct. Biol. 7, 6 (2007).
29. Aono, A. et al. Potent ectopic bone-inducing activity of bone morphogenetic protein-4/7 heterodimer. Biochem. Biophys. Res. Commun. 210, 670-677 (1995).
30. Suzuki, A., Kaneko, E., Ueno, N. & Hemmati-Brivanlou, A. Regulation of epidermal induction by BMP2 and BMP7 signaling. Dev. Biol. 189 112-122 (1997).
31. Nishimatsu, S. & Thomsen, G. H. Ventral mesoderm induction and patterning by bone morphogenetic protein heterodimers in Xenopus embryos. Mech. Dev. 74, 75-88 (1998).
32. Khokha, M. K., Yeh, J., Grammer, T. C. & Harland, R. M. Depletion of three BMP antagonists from Spemann's organizer leads to a catastrophic loss of dorsal structures. Dev. Cell 8, 401-411 (2005).
33. Dal-Pra, S., Furthauer, M., Van-Celst, J., Thisse, B. & Thisse, C. Noggin1 and Follistatinlike2 function redundantly to Chordin to antagonize BMP activity. Dev Biol. 298, 514-526 (2006).
34. Piccolo, S., Sasai, Y., Lu, B. & De Robertis, E. M. Dorsoventral patterning in Xenopus: Inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 86, 589-598 (1996).
35. Zimmerman, L. B., De Jesus-Escobar, J. M. & Harland, R. M. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86, 599-606 (1996).
36. Piccolo, S. et al. The head inducer Cerberus is a multifunctional antagonist of Nodal, BMP and Wnt signals. Nature 397, 707-710 (1999).
37. Piccolo, S. et al. Cleavage of Chordin by Xolloid metalloprotease suggests a role for proteolytic processing in the regulation of Spemann organizer activity. Cell 91, 407-416 (1997).
38. De Robertis, E. M. Spemann's organizer and self-regulation in amphibian embryos. Nat Rev Mol Cell Biol. 7, 296-302 (2006).
39. Nguyen, V. H. et al. Dorsal and intermediate neuronal cell types of the spinal cord are established by a BMP signaling pathway. Development 127, 1209-1220 (2000).
40. Nguyen, V. H. et al. Ventral and lateral regions of the zebrafish gastrula, including the neural crest progenitors, are established by a bmp2b/swirl pathway of genes. Dev Biol. 199, 93-110 (1998).
41. Padgett, K. A. & Sorge, J. A. Creating seamless junctions independent of restriction sites in PCR cloning. Gene 168, 31-35 (1996).
42. Robu, M. E. et al. p53 activation by knockdown technologies. PLoS Genet. 3, e78 (2007).
43. Little, S. C. & Mullins, M. C. Twisted gastrulation promotes BMP signaling in zebrafish dorsal-ventral axial patterning. Development 131, 5825-5835 (2004).
44. Nasevicius, A. & Ekker, S. C. Effective targeted gene 'knockdown' in zebrafish. Nat Genet. 26, 216-20 (2000).