Systems control of BMP morphogen flow in vertebrate embryos

Current Opinion in Genetics and Development

Volumn 21, Issue 6, 2011, Pages 696-703

  Plouhinec, Jean Louis ^a   Zakin, Lise ^a   De Robertis, Edward M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; BONE MORPHOGENETIC PROTEIN RECEPTOR 2; CHORDIN; COLLAGEN TYPE 4; GLYPICAN; NOGGIN; OSTEOGENIC PROTEIN 1; PROTEOHEPARAN SULFATE; TOLLOID METALLOPROTEINASE;

DROSOPHILA; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; FEEDBACK SYSTEM; GASTRULA; MATHEMATICAL MODEL; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; VERTEBRATE; XENOPUS;

ANIMALS; BONE MORPHOGENETIC PROTEINS; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MORPHOGENESIS; SIGNAL TRANSDUCTION; SYSTEMS BIOLOGY; XENOPUS;

ANURA; VERTEBRATA;

EID: 81955160711     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2011.09.001     Document Type: Review

References (65)

1. Plouhinec J.L., De Robertis E.M. Systems biology of the self-regulating morphogenetic gradient of the Xenopus gastrula. Cold Spring Harbor Perspect Biol 2009, 1:a001701.
2. Umulis D., O'Connor M.B., Blair S.S. The extracellular regulation of bone morphogenetic protein signaling. Development 2009, 136:3715-3728.
3. Wu M.Y., Hill C.S. Tgf-beta superfamily signaling in embryonic development and homeostasis. Dev Cell 2009, 16:329-343.
4. De Robertis E.M., Kuroda H. Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu Rev Cell Dev Biol 2004, 20:285-308.
5. Smith W.C., Harland R.M. Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 1992, 70:829-840.
6. Hemmati-Brivanlou A., Kelly O.G., Melton D.A. Follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neuralizing activity. Cell 1994, 77:283-295.
7. Sasai Y., Lu B., Steinbeisser H., Geissert D., Gont L.K., De Robertis E.M. Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes. Cell 1994, 79:779-790.
8. Nakayama N., Han C.E., Scully S., Nishinakamura R., He C., Zeni L., Yamane H., Chang D., Yu D., Yokota T., et al. A novel chordin-like protein inhibitor for bone morphogenetic proteins expressed preferentially in mesenchymal cell lineages. Dev Biol 2001, 232:372-387.
9. Nakayama N., Han C.Y., Cam L., Lee J.I., Pretorius J., Fisher S., Rosenfeld R., Scully S., Nishinakamura R., Duryea D., et al. A novel chordin-like BMP inhibitor, CHL2, expressed preferentially in chondrocytes of developing cartilage and osteoarthritic joint cartilage. Development 2004, 131:229-240.
10. Sasai Y., Lu B., Steinbeisser H., De Robertis E.M. Regulation of neural induction by the Chd and Bmp-4 antagonistic patterning signals in Xenopus. Nature 1995, 377:757.
11. 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 1996, 86:589-598.
12. Zimmerman L.B., De Jesus-Escobar J.M., Harland R.M. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 1996, 86:599-606.
13. Oelgeschläger M., Larrain J., Geissert D., De Robertis E.M. The evolutionarily conserved BMP-binding protein Twisted gastrulation promotes BMP signalling. Nature 2000, 405:757-763.
14. Little S.C., Mullins M.C. Twisted gastrulation promotes BMP signaling in zebrafish dorsal-ventral axial patterning. Development 2004, 131:5825-5835.
15. Xie J., Fisher S. Twisted gastrulation enhances BMP signaling through chordin dependent and independent mechanisms. Development 2005, 132:383-391.
16. Onichtchouk D., Chen Y.G., Dosch R., Gawantka V., Delius H., Massague J., Niehrs C. Silencing of TGF-beta signalling by the pseudoreceptor BAMBI. Nature 1999, 401:480-485.
17. Conley C.A., Silburn R., Singer M.A., Ralston A., Rohwer-Nutter D., Olson D.J., Gelbart W., 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 2000, 127:3947-3959.
18. Serpe M., Umulis D., Ralston A., Chen J., Olson D.J., Avanesov A., Othmer H., O'Connor M.B., Blair S.S. The BMP-binding protein Crossveinless 2 is a short-range, concentration-dependent, biphasic modulator of BMP signaling in Drosophila. Dev Cell 2008, 14:940-953.
19. Zhang J.L., Qiu L.Y., Kotzsch A., Weidauer S., Patterson L., Hammerschmidt M., Sebald W., Mueller T.D. Crystal structure analysis reveals how the Chordin family member crossveinless 2 blocks BMP-2 receptor binding. Dev Cell 2008, 14:739-750.
20. Kelley R., Ren R., Pi X., Wu Y., Moreno I., Willis M., Moser M., Ross M., Podkowa M., Attisano L., et al. A concentration-dependent endocytic trap and sink mechanism converts Bmper from an activator to an inhibitor of Bmp signaling. J Cell Biol 2009, 184:597-609.
21. Ambrosio A.L., Taelman V.F., Lee H.X., Metzinger C.A., Coffinier C., De Robertis E.M. Crossveinless-2 is a BMP feedback inhibitor that binds Chordin/BMP to regulate Xenopus embryonic patterning. Dev Cell 2008, 15:248-260.
22. Zhang J.L., Patterson L.J., Qiu L.Y., Graziussi D., Sebald W., Hammerschmidt M. Binding between Crossveinless-2 and Chordin von Willebrand factor type C domains promotes BMP signaling by blocking Chordin activity. PLoS ONE 2010, 5:e12846.
23. Piccolo S., Agius E., Lu B., Goodman S., Dale L., De Robertis E.M. Cleavage of Chordin by Xolloid metalloprotease suggests a role for proteolytic processing in the regulation of Spemann organizer activity. Cell 1997, 91:407-416.
24. Marques G., Musacchio M., Shimell M.J., Wunnenberg-Stapleton K., Cho K.W., O'Connor M.B. Production of a DPP activity gradient in the early Drosophila embryo through the opposing actions of the SOG and TLD proteins. Cell 1997, 91:417-426.
25. Ferguson E.L., Anderson K.V. Localized enhancement and repression of the activity of the TGF-beta family member, decapentaplegic, is necessary for dorsal-ventral pattern formation in the Drosophila embryo. Development 1992, 114:583-597.
26. Inomata H., Haraguchi T., Sasai Y. Robust stability of the embryonic axial pattern requires a secreted scaffold for chordin degradation. Cell 2008, 134:854-865.
27. Lee H.X., Ambrosio A.L., Reversade B., De Robertis E.M. Embryonic dorsal-ventral signaling: secreted frizzled-related proteins as inhibitors of tolloid proteinases. Cell 2006, 124:147-159.
28. Muraoka O., Shimizu T., Yabe T., Nojima H., Bae Y.K., Hashimoto H., Hibi M. Sizzled controls dorso-ventral polarity by repressing cleavage of the Chordin protein. Nat Cell Biol 2006, 8:329-338.
29. Ploper D., Lee H.X., De Robertis E.M. Dorsal-ventral patterning: Crescent is a dorsally secreted Frizzled-related protein that competitively inhibits Tolloid proteases. Dev Biol 2011, 352:317-328.
30. Lee H.X., Mendes F.A., Plouhinec J.L., De Robertis E.M. Enzymatic regulation of pattern: BMP4 binds CUB domains of Tolloids and inhibits proteinase activity. Genes Dev 2009, 23:2551-2562.
31. Ramirez-Weber F.A., Kornberg T.B. Cytonemes: cellular processes that project to the principal signaling center in Drosophila imaginal discs. Cell 1999, 97:599-607.
32. Greco V., Hannus M., Eaton S. Argosomes: a potential vehicle for the spread of morphogens through epithelia. Cell 2001, 106:633-645.
33. Roy S., Hsiung F., Kornberg T.B. Specificity of Drosophila cytonemes for distinct signaling pathways. Science 2011, 332:354-358.
34. Yan D., Lin X. Shaping morphogen gradients by proteoglycans. Cold Spring Harb Perspect Biol 2009, 1:a002493.
35. Giraldez A.J., Copley R.R., Cohen S.M. HSPG modification by the secreted enzyme Notum shapes the Wingless morphogen gradient. Dev Cell 2002, 2:667-676.
36. Wang X., Harris R.E., Bayston L.J., Ashe H.L. Type IV collagens regulate BMP signalling in Drosophila. Nature 2008, 455:72-77.
37. Vuilleumier R., Springhorn A., Patterson L., Koidl S., Hammerschmidt M., Affolter M., Pyrowolakis G. Control of Dpp morphogen signalling by a secreted feedback regulator. Nat Cell Biol 2010, 12:611-617.
38. Jones C.M., Armes N., Smith J.C. Signalling by TGF-beta family members: short-range effects of Xnr-2 and BMP-4 contrast with the long-range effects of activin. Curr Biol 1996, 6:1468-1475.
39. Ohkawara B., Iemura S., ten Dijke P., Ueno N. Action range of BMP is defined by its N-terminal basic amino acid core. Curr Biol 2002, 12:205-209.
40. Marjoram L., Wright C. Rapid differential transport of Nodal and Lefty on sulfated proteoglycan-rich extracellular matrix regulates left-right asymmetry in Xenopus. Development 2011, 138:475-485.
41. Little S.C., Mullins M.C. Extracellular modulation of BMP activity in patterning the dorsoventral axis. Birth Defects Res C Embryo Today 2006, 78:224-242.
42. Olivares G.H., Carrasco H., Aroca F., Carvallo L., Segovia F., Larrain J. Syndecan-1 regulates BMP signaling and dorso-ventral patterning of the ectoderm during early Xenopus development. Dev Biol 2009, 329:338-349.
43. Dutko J.A., Mullins M.C. SnapShot: BMP signaling in development. Cell 2011, 145. 636-636.e2.
44. Kuo W.J., Digman M.A., Lander A.D. Heparan sulfate acts as a bone morphogenetic protein coreceptor by facilitating ligand-induced receptor hetero-oligomerization. Mol Biol Cell 2010, 21:4028-4041.
45. Dale L., Wardle F.C. A gradient of BMP activity specifies dorsal-ventral fates in early Xenopus embryos. Semin Cell Dev Biol 1999, 10:319-326.
46. De Robertis E.M. Spemann's organizer and self-regulation in amphibian embryos. Nat Rev Mol Cell Biol 2006, 7:296-302.
47. Reversade B., De Robertis E.M. Regulation of ADMP and BMP2/4/7 at opposite embryonic poles generates a self-regulating morphogenetic field. Cell 2005, 123:1147-1160.
48. De Robertis E.M. Spemann's organizer and the self-regulation of embryonic fields. Mech Dev 2009, 126:925-941.
49. Eldar A., Dorfman R., Weiss D., Ashe H., Shilo B.Z., Barkai N. Robustness of the BMP morphogen gradient in Drosophila embryonic patterning. Nature 2002, 419:304-308.
50. Wang Y.C., Ferguson E.L. Spatial bistability of Dpp-receptor interactions during Drosophila dorsal-ventral patterning. Nature 2005, 434:229-234.
51. 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 2005, 120:873-886.
52. Zakin L., Chang E.Y., Plouhinec J.L., De Robertis E.M. Crossveinless-2 is required for the relocalization of Chordin protein within the vertebral field in mouse embryos. Dev Biol 2010, 347:204-215.
53. Turing A.M. The chemical basis of morphogenesis. Philos Trans R Soc Lond 1952, 237:37-72.
54. Gierer A., Meinhardt H. A theory of biological pattern formation. Kybernetik 1972, 12:30-39.
55. Meinhardt H. Models for the generation and interpretation of gradients. Cold Spring Harb Perspect Biol 2009, 1:a001362.
56. Ben-Zvi D., Shilo B.Z., Fainsod A., Barkai N. Scaling of the BMP activation gradient in Xenopus embryos. Nature 2008, 453:1205-1211.
57. Zhang J.L., Huang Y., Qiu L.Y., Nickel J., Sebald W. von Willebrand factor type C domain-containing proteins regulate bone morphogenetic protein signaling through different recognition mechanisms. J Biol Chem 2007, 282:20002-20014.
58. Paulsen M., Legewie S., Eils R., Karaulanov E., Niehrs C. Negative feedback in the bone morphogenetic protein 4 (BMP4) synexpression group governs its dynamic signaling range and canalizes development. Proc Natl Acad Sci USA 2011, 108:10202-10207.
59. Lander A.D. Pattern, growth, and control. Cell 2011, 144:955-969.
60. Ben-Zvi D., Barkai N. Scaling of morphogen gradients by an expansion-repression integral feedback control. Proc Natl Acad Sci USA 2010, 107:6924-6929.
61. Spemann H., Mangold H. Induction of embryonic primordial by implantation of organizers from a different species. Roux's Arch Entw Mech 1924, 100:599-638. (reprinted and translated in Int J Dev Biol 2001, 45:13-31).
62. Umulis D.M., Shimmi O., O'Connor M.B., Othmer H.G. Organism-scale modeling of early Drosophila patterning via bone morphogenetic proteins. Dev Cell 2010, 18:260-274.
63. Wartlick O., Mumcu P., Kicheva A., Bittig T., Seum C., Julicher F., Gonzalez-Gaitan M. Dynamics of Dpp signaling and proliferation control. Science 2011, 331:1154-1159.
64. Eivers E., Fuentealba L.C., De Robertis E.M. Integrating positional information at the level of Smad1/5/8. Curr Opin Genet Dev 2008, 18:304-310.
65. Massague J., Seoane J., Wotton D. Smad transcription factors. Genes Dev 2005, 19:2783-2810.