Spatial regulation of BMP activity

FEBS Letters

Volumn 586, Issue 14, 2012, Pages 1929-1941

  Ramel, Marie Christine ^a   Hill, Caroline S ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

BMP; Gradient; Morphogen; Signalling; Smad; TGF superfamily

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 5; BONE MORPHOGENETIC PROTEIN 6; BONE MORPHOGENETIC PROTEIN 8; BONE MORPHOGENETIC PROTEIN RECEPTOR; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; DECAPENTAPLEGIC PROTEIN; GROWTH FACTOR; MORPHOGEN; OSTEOGENIC PROTEIN 1; RECEPTOR REGULATED SMAD PROTEIN; SCLEROPROTEIN; SMAD PROTEIN; SMAD1 PROTEIN; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

BINDING AFFINITY; BONE MORPHOGENETIC PROTEIN GENE; CYTOPLASM; EMBRYO DEATH; EXTRACELLULAR SPACE; GENE; GENE EXPRESSION REGULATION; HUMAN; LIGAND BINDING; MEMBRANE BINDING; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STABILITY; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; SUMOYLATION; TRANSCRIPTION REGULATION; TRANSLATION REGULATION;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL NUCLEUS; DEVELOPMENTAL BIOLOGY; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; LIGANDS; MICE; MODELS, BIOLOGICAL; PHOSPHORYLATION; PROTEIN BINDING; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; XENOPUS LAEVIS; ZEBRAFISH;

EID: 84862758164     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2012.02.035     Document Type: Review

References (134)

1. K. Miyazono, Y. Kamiya, and M. Morikawa Bone morphogenetic protein receptors and signal transduction J. Biochem. 147 2010 35 51
2. I.L. Blitz, and K.W. Cho Finding partners: how BMPs select their targets Dev. Dyn. 238 2009 1321 1331
3. M. Blanco Calvo, V. Bolos Fernandez, V. Medina Villaamil, G. Aparicio Gallego, S. Diaz Prado, and E. Grande Pulido Biology of BMP signalling and cancer Clin. Transl. Oncol. 11 2009 126 137
4. M.B. O'Connor, D. Umulis, H.G. Othmer, and S.S. Blair Shaping BMP morphogen gradients in the Drosophila embryo and pupal wing Development 133 2006 183 193
5. J.L. Plouhinec, L. Zakin, and E.M. De Robertis Systems control of BMP morphogen flow in vertebrate embryos Curr. Opin. Genet. Dev. 21 2011 696 703
6. Y.G. Langdon, and M.C. Mullins Maternal and zygotic control of zebrafish dorsoventral axial patterning Annu. Rev. Genet. 45 2011 357 377
7. J.D. Benazet, and R. Zeller Vertebrate limb development: moving from classical morphogen gradients to an integrated 4-dimensional patterning system Cold Spring Harb. Perspect. Biol. 1 2009 a001339
8. B. Robert Bone morphogenetic protein signaling in limb outgrowth and patterning Dev. Growth Differ. 49 2007 455 468
9. M.L. Basch, and M. Bronner-Fraser Neural crest inducing signals Adv. Exp. Med. Biol. 589 2006 24 31
10. R.F. Collery, and B.A. Link Dynamic smad-mediated BMP signaling revealed through transgenic zebrafish Dev. Dyn. 240 2011 712 722
11. D.W. Laux, J.A. Febbo, and B.L. Roman Dynamic analysis of BMP-responsive smad activity in live zebrafish embryos Dev. Dyn. 240 2011 682 694
12. C. Alexander Combinatorial roles for BMPs and Endothelin 1 in patterning the dorsal-ventral axis of the craniofacial skeleton Development 138 2011 5135 5146
13. M.Y. Wu, M.C. Ramel, M. Howell, and C.S. Hill SNW1 is a critical regulator of spatial BMP activity, neural plate border formation, and neural crest specification in vertebrate embryos PLoS Biol. 9 2011 e1000593
14. R.M. Monteiro, S.M. de Sousa Lopes, M. Bialecka, S. de Boer, A. Zwijsen, and C.L. Mummery Real time monitoring of BMP Smads transcriptional activity during mouse development Genesis 46 2008 335 346
15. F. Lapraz, L. Besnardeau, and T. Lepage Patterning of the dorsal-ventral axis in echinoderms: insights into the evolution of the BMP-chordin signaling network PLoS Biol. 7 2009 e1000248
16. A. Kicheva, and M. Gonzalez-Gaitan The Decapentaplegic morphogen gradient: a precise definition Curr. Opin. Cell Biol. 20 2008 137 143
17. K.W. Rogers, and A.F. Schier Morphogen gradients: from generation to interpretation Annu. Rev. Cell Dev. Biol. 27 2011 377 407
18. M.C. Gibson, D.A. Lehman, and G. Schubiger Lumenal transmission of decapentaplegic in Drosophila imaginal discs Dev. Cell 3 2002 451 460
19. A.A. Teleman, and S.M. Cohen Dpp gradient formation in the Drosophila wing imaginal disc Cell 103 2000 971 980
20. E.V. Entchev, A. Schwabedissen, and M. Gonzalez-Gaitan Gradient formation of the TGF-β homolog Dpp Cell 103 2000 981 991
21. H. Tanimoto, S. Itoh, P. ten Dijke, and T. Tabata Hedgehog creates a gradient of DPP activity in Drosophila wing imaginal discs Mol. Cell 5 2000 59 71
22. E. Bangi, and 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 2006 178 193
23. Y. Ogiso, K. Tsuneizumi, N. Masuda, M. Sato, and T. Tabata Robustness of the Dpp morphogen activity gradient depends on negative feedback regulation by the inhibitory Smad, Dad Dev. Growth Differ. 53 2011 668 678
24. B. Schmierer, and C.S. Hill TGF-β SMAD signal transduction: molecular specificity and functional flexibility Nat. Rev. Mol. Cell Biol. 8 2007 970 982
25. Y. Cui, F. Jean, G. Thomas, and J.L. Christian BMP-4 is proteolytically activated by furin and/or PC6 during vertebrate embryonic development EMBO J. 17 1998 4735 4743
26. D.B. Constam, and E.J. Robertson Regulation of bone morphogenetic protein activity by pro domains and proprotein convertases J. Cell Biol. 144 1999 139 149
27. M. Ehrlich, D. Horbelt, B. Marom, P. Knaus, and Y.I. Henis Homomeric and heteromeric complexes among TGF-β and BMP receptors and their roles in signaling Cell. Signal. 23 2011 1424 1432
28. X.H. Feng, and R. Derynck Specificity and versatility in TGF-β signaling through Smads Annu. Rev. Cell Dev. Biol. 21 2005 659 693
29. A.C. Daly, R.A. Randall, and 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 2008 6889 6902
30. S.J. Arnold, S. Maretto, A. Islam, E.K. Bikoff, and E.J. Robertson Dose-dependent Smad1, Smad5 and Smad8 signaling in the early mouse embryo Dev. Biol. 296 2006 104 118
31. Z. Huang, D. Wang, K. Ihida-Stansbury, P.L. Jones, and J.F. Martin Defective pulmonary vascular remodeling in Smad8 mutant mice Hum. Mol. Genet. 18 2009 2791 2801
32. M. Kretzschmar, F. Liu, A. Hata, J. Doody, and J. Massague The TGF-β family mediator Smad1 is phosphorylated directly and activated functionally by the BMP receptor kinase Genes Dev. 11 1997 984 995
33. S. Gao, J. Steffen, and A. Laughon Dpp-responsive silencers are bound by a trimeric Mad-Medea complex J. Biol. Chem. 280 2005 36158 36164
34. G. Pyrowolakis, B. Hartmann, B. Muller, K. Basler, and M. Affolter A simple molecular complex mediates widespread BMP-induced repression during Drosophila development Dev. Cell 7 2004 229 240
35. T. Nakahiro, H. Kurooka, K. Mori, K. Sano, and Y. Yokota Identification of BMP-responsive elements in the mouse Id2 gene Biochem. Biophys. Res. Commun. 399 2010 416 421
36. A. Weiss, E. Charbonnier, E. Ellertsdottir, A. Tsirigos, C. Wolf, R. Schuh, G. Pyrowolakis, and M. Affolter A conserved activation element in BMP signaling during Drosophila development Nat. Struct. Mol. Biol. 17 2010 69 76
37. H. Dai The zinc finger protein schnurri acts as a Smad partner in mediating the transcriptional response to decapentaplegic Dev. Biol. 227 2000 373 387
38. L.C. Yao Schnurri transcription factors from Drosophila and vertebrates can mediate Bmp signaling through a phylogenetically conserved mechanism Development 133 2006 4025 4034
39. S. Ross, and C.S. Hill How the Smads regulate transcription Int. J. Biochem. Cell Biol. 40 2008 383 408
40. M.Y. Wu, and C.S. Hill TGF-β superfamily signaling in embryonic development and homeostasis Dev. Cell 16 2009 329 343
41. S.T. Lee-Hoeflich, C.G. Causing, M. Podkowa, X. Zhao, J.L. Wrana, and L. Attisano Activation of LIMK1 by binding to the BMP receptor, BMPRII, regulates BMP-dependent dendritogenesis EMBO J. 23 2004 4792 4801
42. L. Wolpert, T. Jessell, P. Lawrence, E. Meyerowitz, E. Robertson, and J. Smith Principles of Development 2007 Oxford University Press Oxford
43. K.M. Cadigan Regulating morphogen gradients in the Drosophila wing Semin. Cell Dev. Biol. 13 2002 83 90
44. M. Zecca, K. Basler, and G. Struhl Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing Development 121 1995 2265 2278
45. S. Sidi, C. Goutel, N. Peyrieras, and F.M. Rosa Maternal induction of ventral fate by zebrafish radar Proc. Natl. Acad. Sci. USA 100 2003 3315 3320
46. G. Reim, and M. Brand Maternal control of vertebrate dorsoventral axis formation and epiboly by the POU domain protein Spg/Pou2/Oct4 Development 133 2006 2757 2770
47. T. Leung, J. Bischof, I. Soll, D. Niessing, D. Zhang, J. Ma, H. Jackle, and W. Driever Bozozok directly represses bmp2b transcription and mediates the earliest dorsoventral asymmetry of bmp2b expression in zebrafish Development 130 2003 3639 3649
48. M. Furthauer, J. Van Celst, C. Thisse, and B. Thisse Fgf signalling controls the dorsoventral patterning of the zebrafish embryo Development 131 2004 2853 2864
49. B. Schmid, M. Fürthauer, S.A. Connors, J. Trout, B. Thisse, C. Thisse, and M.C. Mullins Equivalent genetic roles for bmp7/snailhouse and bmp2b/swirl in dorsoventral pattern formation Development 127 2000 957 967
50. S. Sopory, S. Kwon, M. Wehrli, and J.L. Christian Regulation of Dpp activity by tissue-specific cleavage of an upstream site within the prodomain Dev. Biol. 346 2010 102 112
51. D.C. Goldman, R. Hackenmiller, T. Nakayama, S. Sopory, C. Wong, H. Kulessa, and J.L. Christian Mutation of an upstream cleavage site in the BMP4 prodomain leads to tissue-specific loss of activity Development 133 2006 1933 1942
52. E. Valera, M.J. Isaacs, Y. Kawakami, J.C. Izpisua Belmonte, and S. Choe BMP-2/6 heterodimer is more effective than BMP-2 or BMP-6 homodimers as inductor of differentiation of human embryonic stem cells PLoS ONE 5 2010 e11167
53. 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
54. S.J. Butler, and J. Dodd A role for BMP heterodimers in roof plate-mediated repulsion of commissural axons Neuron 38 2003 389 401
55. 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
56. S.C. Little, and M.C. Mullins Bone morphogenetic protein heterodimers assemble heteromeric type I receptor complexes to pattern the dorsoventral axis Nat. Cell Biol. 11 2009 637 643
57. O. Khalsa, J.W. Yoon, S. Torres-Schumann, and 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 1998 2723 2734
58. R.P. Ray, and K.A. Wharton Context-dependent relationships between the BMPs gbb and dpp during development of the Drosophila wing imaginal disk Development 128 2001 3913 3925
59. C.C. Rider, and B. Mulloy Bone morphogenetic protein and growth differentiation factor cytokine families and their protein antagonists Biochem. J. 429 2010 1 12
60. H. Araujo, M.R. Fontenele, and R.N. da Fonseca Position matters: variability in the spatial pattern of BMP modulators generates functional diversity Genesis 49 2011 698 718
61. L. Zakin, and E.M. De Robertis Extracellular regulation of BMP signaling Curr. Biol. 20 2010 R89 92
62. D. Umulis, M.B. O'Connor, and S.S. Blair The extracellular regulation of bone morphogenetic protein signaling Development 136 2009 3715 3728
63. Raftery, L.A. and Umulis, D.M. (in press). Regulation of BMP activity and range in Drosophila wing development. Curr. Opin. Cell Biol, doi:10.1016/j.ceb.2011.11.004.
64. D. Yan, and X. Lin Shaping morphogen gradients by proteoglycans Cold Spring Harb. Perspect. Biol. 1 2009 a002493
65. J.L. Erickson Formation and maintenance of morphogen gradients: an essential role for the endomembrane system in Drosophila melanogaster wing development Fly (Austin) 5 2011 266 271
66. M. Fujise, S. Takeo, K. Kamimura, T. Matsuo, T. Aigaki, S. Izumi, and H. Nakato Dally regulates Dpp morphogen gradient formation in the Drosophila wing Development 130 2003 1515 1522
67. G.H. Baeg, E.M. Selva, R.M. Goodman, R. Dasgupta, and N. Perrimon The Wingless morphogen gradient is established by the cooperative action of Frizzled and Heparan Sulfate Proteoglycan receptors Dev. Biol. 276 2004 89 100
68. D. Onichtchouk, Y.G. Chen, R. Dosch, V. Gawantka, H. Delius, J. Massague, and C. Niehrs Silencing of TGF-β signalling by the pseudoreceptor BAMBI Nature 401 1999 480 485
69. M. Tsang, R. Kim, M.P. de Caestecker, T. Kudoh, A.B. Roberts, and I.B. Dawid Zebrafish nma is involved in TGFβ family signaling Genesis 28 2000 47 57
70. L. Grotewold, M. Plum, R. Dildrop, T. Peters, and U. Ruther Bambi is coexpressed with Bmp-4 during mouse embryogenesis Mech. Dev. 100 2001 327 330
71. N. Higashihori, Y. Song, and J.M. Richman Expression and regulation of the decoy bone morphogenetic protein receptor BAMBI in the developing avian face Dev. Dyn. 237 2008 1500 1508
72. J. Chen, J.O. Bush, C.E. Ovitt, Y. Lan, and R. Jiang The TGF-β pseudoreceptor gene Bambi is dispensable for mouse embryonic development and postnatal survival Genesis 45 2007 482 486
73. E.M. De Robertis, and H. Kuroda Dorsal-ventral patterning and neural induction in Xenopus embryos Annu. Rev. Cell Dev. Biol. 20 2004 285 308
74. Dutko, J.A. and Mullins, M.C. (2011). SnapShot: BMP signaling in development. Cell 145, 636-636.e2.
75. S. Srinivasan, K.E. Rashka, and E. Bier Creation of a Sog morphogen gradient in the Drosophila embryo Dev. Cell 2 2002 91 101
76. S.A. Connors, J. Trout, M. Ekker, and M.C. Mullins The role of tolloid/mini fin in dorsoventral pattern formation of the zebrafish embryo Development 126 1999 3119 3130
77. S.A. Connors, J.A. Tucker, and M.C. Mullins Temporal and spatial action of tolloid (mini fin) and chordin to pattern tail tissues Dev. Biol. 293 2006 191 202
78. M. Serpe The BMP-binding protein Crossveinless 2 is a short-range, concentration-dependent, biphasic modulator of BMP signaling in Drosophila Dev. Cell 14 2008 940 953
79. M. Moser BMPER, a novel endothelial cell precursor-derived protein, antagonizes bone morphogenetic protein signaling and endothelial cell differentiation Mol. Cell. Biol. 23 2003 5664 5679
80. F. Rentzsch, J. Zhang, C. Kramer, W. Sebald, and M. Hammerschmidt Crossveinless 2 is an essential positive feedback regulator of Bmp signaling during zebrafish gastrulation Development 133 2006 801 811
81. M. Ikeya, M. Kawada, H. Kiyonari, N. Sasai, K. Nakao, Y. Furuta, and Y. Sasai Essential pro-Bmp roles of crossveinless 2 in mouse organogenesis Development 133 2006 4463 4473
82. A. Ralston, and S.S. Blair Long-range Dpp signaling is regulated to restrict BMP signaling to a crossvein competent zone Dev. Biol. 280 2005 187 200
83. R. Vuilleumier, A. Springhorn, L. Patterson, S. Koidl, M. Hammerschmidt, M. Affolter, and G. Pyrowolakis Control of Dpp morphogen signalling by a secreted feedback regulator Nat. Cell Biol. 12 2010 611 617
84. M. Szuperak, S. Salah, E.J. Meyer, U. Nagarajan, A. Ikmi, and M.C. Gibson Feedback regulation of Drosophila BMP signaling by the novel extracellular protein larval translucida Development 138 2011 715 724
85. F. Ramirez, and D.B. Rifkin Extracellular microfibrils: contextual platforms for TGFβ and BMP signaling Curr. Opin. Cell Biol. 21 2009 616 622
86. X. Wang, R.E. Harris, L.J. Bayston, and H.L. Ashe Type IV collagens regulate BMP signalling in Drosophila Nature 455 2008 72 77
87. H.L. Ashe Type IV collagens and Dpp positive and negative regulators of signaling Fly (Austin) 2 2008 313 315
88. C.M. Jones, N. Armes, and J.C. Smith Signalling by TGF-β family members: short-range effects of Xnr-2 and BMP-4 contrast with the long-range effects of activin Curr. Biol. 6 1996 1468 1475
89. P. Muller, and A.F. Schier Extracellular movement of signaling molecules Dev. Cell 21 2011 145 158
90. M. Affolter, and K. Basler Cell biology. Cytonemes show their colors Science 332 2011 312 313
91. F. Hsiung, F.A. Ramirez-Weber, D.D. Iwaki, and T.B. Kornberg Dependence of Drosophila wing imaginal disc cytonemes on Decapentaplegic Nature 437 2005 560 563
92. Roy, S. and Kornberg, T.B. (2011). Direct delivery mechanisms of morphogen dispersion. Sci. Signal. 4, pt8.
93. M. Gonzalez-Gaitan Endocytic trafficking during Drosophila development Mech. Dev. 120 2003 1265 1282
94. G. Schwank, S. Dalessi, S.F. Yang, R. Yagi, A.M. de Lachapelle, M. Affolter, S. Bergmann, and K. Basler Formation of the long range Dpp morphogen gradient PLoS Biol. 9 2011 e1001111
95. M.A. Crickmore, and R.S. Mann Hox control of organ size by regulation of morphogen production and mobility Science 313 2006 63 68
96. B.V. Shravage, G. Altmann, M. Technau, and S. Roth The role of Dpp and its inhibitors during eggshell patterning in Drosophila Development 134 2007 2261 2271
97. E.Y. Mantrova, R.A. Schulz, and T. Hsu Oogenic function of the myogenic factor D-MEF2: negative regulation of the decapentaplegic receptor gene thick veins Proc. Natl. Acad. Sci. USA 96 1999 11889 11894
98. N. Yakoby A combinatorial code for pattern formation in Drosophila oogenesis Dev. Cell 15 2008 725 737
99. J. Lembong, N. Yakoby, and S.Y. Shvartsman Pattern formation by dynamically interacting network motifs Proc. Natl. Acad. Sci. USA 106 2009 3213 3218
100. E. Bangi, and K. Wharton Dual function of the Drosophila Alk1/Alk2 ortholog Saxophone shapes the Bmp activity gradient in the wing imaginal disc Development 133 2006 3295 3303
101. S. Chen, S. Wang, and T. Xie Restricting self-renewal signals within the stem cell niche: multiple levels of control Curr. Opin. Genet. Dev. 21 2011 684 689
102. L. Xia The Fused/Smurf complex controls the fate of Drosophila germline stem cells by generating a gradient BMP response Cell 143 2010 978 990
103. M. Nikaido, M. Tada, H. Takeda, A. Kuroiwa, and N. Ueno In vivo analysis using variants of zebrafish BMPR-IA: range of action and involvement of BMP in ectoderm patterning Development 126 1999 181 190
104. G. Sapkota, C. Alarcon, F.M. Spagnoli, A.H. Brivanlou, and J. Massague Balancing BMP signaling through integrated inputs into the Smad1 linker Mol. Cell 25 2007 441 454
105. L.C. Fuentealba, E. Eivers, A. Ikeda, C. Hurtado, H. Kuroda, E.M. Pera, and E.M. De Robertis Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal Cell 131 2007 980 993
106. Eivers, E., Demagny, H., Choi, R.H. and De Robertis, E.M. (2011). Phosphorylation of Mad controls competition between wingless and BMP signaling. Sci. Signal. 4, ra68.
107. Y.A. Zeng, M. Rahnama, S. Wang, W. Sosu-Sedzorme, and E.M. Verheyen Drosophila Nemo antagonizes BMP signaling by phosphorylation of Mad and inhibition of its nuclear accumulation Development 134 2007 2061 2071
108. E.M. Verheyen, I. Mirkovic, S.J. MacLean, C. Langmann, B.C. Andrews, and C. MacKinnon The tissue polarity gene nemo carries out multiple roles in patterning during Drosophila development Mech. Dev. 101 2001 119 132
109. J.R. Gareau, and C.D. Lima The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition Nat. Rev. Mol. Cell Biol. 11 2010 861 871
110. W.O. Miles Medea SUMOylation restricts the signaling range of the Dpp morphogen in the Drosophila embryo Genes Dev. 22 2008 2578 2590
111. S.J. Wharton, S.P. Basu, and H.L. Ashe Smad affinity can direct distinct readouts of the embryonic extracellular Dpp gradient in Drosophila Curr. Biol. 14 2004 1550 1558
112. M. Affolter, T. Marty, M.A. Vigano, and A. Jazwinska Nuclear interpretation of Dpp signaling in Drosophila EMBO J. 20 2001 3298 3305
113. R. Barrio, and J.F. de Celis Regulation of spalt expression in the Drosophila wing blade in response to the Decapentaplegic signaling pathway Proc. Natl. Acad. Sci. USA 101 2004 6021 6026
114. G. Campbell, and A. Tomlinson Transducing the Dpp morphogen gradient in the wing of Drosophila: regulation of Dpp targets by brinker Cell 96 1999 553 562
115. Y.C. Wang, and E.L. Ferguson Spatial bistability of Dpp-receptor interactions during Drosophila dorsal-ventral patterning Nature 434 2005 229 234
116. J. Bakkers, M. Hild, C. Kramer, M. Furutani-Seiki, and M. Hammerschmidt Zebrafish DeltaNp63 is a direct target of Bmp signaling and encodes a transcriptional repressor blocking neural specification in the ventral ectoderm Dev. Cell 2 2002 617 627
117. K.A. Henningfeld, S. Rastegar, G. Adler, and W. Knochel Smad1 and Smad4 are components of the bone morphogenetic protein-4 (BMP-4)-induced transcription complex of the Xvent-2B promoter J. Biol. Chem. 275 2000 21827 21835
118. C. Alarcon Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF-β pathways Cell 139 2009 757 769
119. T. Fei Genome-wide mapping of SMAD target genes reveals the role of BMP signaling in embryonic stem cell fate determination Genome Res. 20 2010 36 44
120. D.A. Peiffer, A. Von Bubnoff, Y. Shin, A. Kitayama, M. Mochii, N. Ueno, and K.W. Cho A Xenopus DNA microarray approach to identify novel direct BMP target genes involved in early embryonic development Dev. Dyn. 232 2005 445 456
121. A. von Bubnoff, D.A. Peiffer, I.L. Blitz, T. Hayata, S. Ogata, Q. Zeng, M. Trunnell, and K.W. Cho Phylogenetic footprinting and genome scanning identify vertebrate BMP response elements and new target genes Dev. Biol. 281 2005 210 226
122. C. Martin-Castellanos, and B.A. Edgar A characterization of the effects of Dpp signaling on cell growth and proliferation in the Drosophila wing Development 129 2002 1003 1013
123. D. Rogulja, and K.D. Irvine Regulation of cell proliferation by a morphogen gradient Cell 123 2005 449 461
124. O. Wartlick, P. Mumcu, A. Kicheva, T. Bittig, C. Seum, F. Julicher, and M. Gonzalez-Gaitan Dynamics of Dpp signaling and proliferation control Science 331 2011 1154 1159
125. F. Hamaratoglu, A.M. de Lachapelle, G. Pyrowolakis, S. Bergmann, and M. Affolter Dpp signaling activity requires Pentagone to scale with tissue size in the growing Drosophila wing imaginal disc PLoS Biol. 9 2011 e1001182
126. Baena-Lopez, L.A., Nojima, H. and Vincent, J.P. (in press). Integration of morphogen signalling within the growth regulatory network. Curr. Opin. Cell Biol, doi:10.1016/j.ceb.2011.12.010.
127. L.A. Brosens, D. Langeveld, W.A. van Hattem, F.M. Giardiello, and G.J. Offerhaus Juvenile polyposis syndrome World J. Gastroenterol. 17 2011 4839 4844
128. D.W. Walsh, C. Godson, D.P. Brazil, and F. Martin Extracellular BMP-antagonist regulation in development and disease: tied up in knots Trends Cell Biol. 20 2010 244 256
129. J.L. Plouhinec, and E.M. De Robertis Systems biology of the self-regulating morphogenetic gradient of the Xenopus gastrula Cold Spring Harb. Perspect. Biol. 1 2009 a001701
130. C.R. French, T. Erickson, D.V. French, D.B. Pilgrim, and A.J. Waskiewicz Gdf6a is required for the initiation of dorsal-ventral retinal patterning and lens development Dev. Biol. 333 2009 37 47
131. B. Muller, B. Hartmann, G. Pyrowolakis, M. Affolter, and K. Basler Conversion of an extracellular Dpp/BMP morphogen gradient into an inverse transcriptional gradient Cell 113 2003 221 233
132. J. Shen, C. Dahmann, and G.O. Pflugfelder Spatial discontinuity of optomotor-blind expression in the Drosophila wing imaginal disc disrupts epithelial architecture and promotes cell sorting BMC Dev. Biol. 10 2010 23
133. S.S. Blair Wing vein patterning in Drosophila and the analysis of intercellular signaling Annu. Rev. Cell Dev. Biol. 23 2007 293 319
134. C.A. Conley, R. Silburn, M.A. Singer, A. Ralston, D. Rohwer-Nutter, D.J. Olson, W. Gelbart, and S.S. Blair 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 127 2000 3947 3959