BMP signaling and early embryonic patterning

Cytokine and Growth Factor Reviews

Volumn 16, Issue 3 SPEC. ISS., 2005, Pages 265-278

  Kishigami, Satoshi ^a,b   Mishina, Yuji ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

BMP; Embryogenesis; Embryonic patterning; Gastrulation; Receptor; TGF

Indexed keywords

ACTIVIN; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 8; BONE MORPHOGENETIC PROTEIN RECEPTOR; BONE MORPHOGENETIC PROTEIN RECEPTOR 1 A; GROWTH DIFFERENTIATION FACTOR 5; GROWTH DIFFERENTIATION FACTOR 6; LIGAND; PROTEIN; PROTEIN ACVR 1; PROTEIN NODAL; SMAD1 PROTEIN; SMAD3 PROTEIN; SMAD5 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

CHICKEN; EMBRYO DEVELOPMENT; FROG; GASTRULATION; GERM LAYER; KNOCKOUT GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION;

EID: 21344433063     PISSN: 13596101     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cytogfr.2005.04.002     Document Type: Article

References (163)

1. M.R. Urist Bone: formation by autoinduction Science 150 1965 893 899
2. D.M. Kingsley The TGF-beta superfamily: new members, new receptors, and new genetic tests of function in different organisms Genes Dev 8 1994 133 146
3. G.Q. Zhao Consequences of knocking out BMP signaling in the mouse Genesis 35 2003 43 56
4. J.M. Wozney The bone morphogenetic protein family and osteogenesis Mol Reprod Dev 32 1992 160 167
5. T.K. Sampath, and A.H. Reddi Dissociative extraction and reconstitution of extracellular matrix components involved in local bone differentiation Proc Natl Acad Sci USA 78 1981 7599 7603
6. A.H. Reddi Bone and cartilage differentiation Curr Opin Genet Dev 4 1994 737 744
7. B.L. Hogan Bone morphogenetic proteins in development Curr Opin Genet Dev 6 1996 432 438
8. M. Whitman Smads and early developmental signaling by the TGFbeta superfamily Genes Dev 12 1998 2445 2462
9. Y. Mishina Function of bone morphogenetic protein signaling during mouse development Front Biosci 8 2003 d855 d869
10. R.P. Ray, K. Arora, C. Nusslein-Volhard, and W.M. Gelbart The control of cell fate along the dorsal-ventral axis of the Drosophila embryo Development 113 1991 35 54
11. L. Dale, G. Howes, B.M. Price, and J.C. Smith Bone morphogenetic protein 4: a ventralizing factor in early Xenopus development Development 115 1992 573 585
12. C.M. Jones, K.M. Lyons, P.M. Lapan, C.V. Wright, and B.L. Hogan DVR-4 (bone morphogenetic protein-4) as a posterior-ventralizing factor in Xenopus mesoderm induction Development 115 1992 639 647
13. J.L. Wrana, L. Attisano, R. Wieser, F. Ventura, and J. Massague Mechanism of activation of the TGF-beta receptor Nature 370 1994 341 347
14. C.H. Heldin, K. Miyazono, and P. ten Dijke TGF-beta signalling from cell membrane to nucleus through SMAD proteins Nature 390 1997 465 471
15. P. Franzen, P. ten Dijke, and H. Ichijo Cloning of a TGF beta type I receptor that forms a heteromeric complex with the TGF beta type II receptor Cell 75 1993 681 692
16. J. Carcamo, F.M. Weis, and F. Ventura Type I receptors specify growth-inhibitory and transcriptional responses to transforming growth factor beta and activin Mol Cell Biol 14 1994 3810 3821
17. J. Massague TGFbeta signaling: receptors, transducers, and Mad proteins Cell 85 1996 947 950
18. M. de Caestecker The transforming growth factor-beta superfamily of receptors Cytokine Growth Factor Rev 15 2004 1 11
19. G. Giudice Conserved cellular and molecular mechanisms in development Cell Biol Int 25 2001 1081 1090
20. Y. Sasai Regulation of neural determination by evolutionarily conserved signals: anti-BMP factors and what next? Curr Opin Neurobiol 11 2001 22 26
21. S. Piccolo, E. Agius, and L. Leyns The head inducer Cerberus is a multifunctional antagonist of Nodal BMP and Wnt signals Nature 397 1999 707 710
22. J.A. Belo, D. Bachiller, and E. Agius Cerberus-like is a secreted BMP and nodal antagonist not essential for mouse development Genesis 26 2000 265 270
23. R.M. Anderson, A.R. Lawrence, R.W. Stottmann, D. Bachiller, and J. Klingensmith Chordin and noggin promote organizing centers of forebrain development in the mouse Development 129 2002 4975 4987
24. D. Bachiller, J. Klingensmith, and C. Kemp The organizer factors Chordin and Noggin are required for mouse forebrain development Nature 403 2000 658 661
25. D. Bachiller, J. Klingensmith, and N. Shneyder The role of chordin/Bmp signals in mammalian pharyngeal development and DiGeorge syndrome Development 130 2003 3567 3578
26. W. Shawlot, J. Min Deng, M. Wakamiya, and R.R. Behringer The cerberus-related gene, Cerr1, is not essential for mouse head formation Genesis 26 2000 253 258
27. P.P. Tam, and R.R. Behringer Mouse gastrulation: the formation of a mammalian body plan Mech Dev 68 1997 3 25
28. R.S. Beddington, and E.J. Robertson Axis development and early asymmetry in mammals Cell 96 1999 195 209
29. R.R. Behringer, M. Wakamiya, T.E. Tsang, and P.P. Tam A flattened mouse embryo: leveling the playing field Genesis 28 2000 23 30
30. J. Rossant, and P.P. Tam Emerging asymmetry and embryonic patterning in early mouse development Dev Cell 7 2004 155 164
31. C.C. Lu, J. Brennan, and E.J. Robertson From fertilization to gastrulation: axis formation in the mouse embryo Curr Opin Genet Dev 11 2001 384 392
32. P.Q. Thomas, A. Brown, and R.S. Beddington Hex: a homeobox gene revealing peri-implantation asymmetry in the mouse embryo and an early transient marker of endothelial cell precursors Development 125 1998 85 94
33. J.A. Rivera-Perez, J. Mager, and T. Magnuson Dynamic morphogenetic events characterize the mouse visceral endoderm Dev Biol 261 2003 470 487
34. S. Srinivas, T. Rodriguez, M. Clements, J.C. Smith, and R.S. Beddington Active cell migration drives the unilateral movements of the anterior visceral endoderm Development 131 2004 1157 1164
35. A. Nagy, and J. Rossant Chimaeras and mosaics for dissecting complex mutant phenotypes Int J Dev Biol 45 2001 577 582
36. A. Nagy Cre recombinase: the universal reagent for genome tailoring Genesis 26 2000 99 109
37. G. Winnier, M. Blessing, P.A. Labosky, and B.L. Hogan Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse Genes Dev 9 1995 2105 2116
38. K.A. Lawson, N.R. Dunn, and B.A. Roelen Bmp4 is required for the generation of primordial germ cells in the mouse embryo Genes Dev 13 1999 424 436
39. Y. Ying, X.M. Liu, A. Marble, K.A. Lawson, and G.Q. Zhao Requirement of Bmp8b for the generation of primordial germ cells in the mouse Mol Endocrinol 14 2000 1053 1063
40. Y. Ying, and G.Q. Zhao Cooperation of endoderm-derived BMP2 and extraembryonic ectoderm-derived BMP4 in primordial germ cell generation in the mouse Dev Biol 232 2001 484 492
41. T. Fujiwara, D.B. Dehart, K.K. Sulik, and B.L. Hogan Distinct requirements for extra-embryonic and embryonic bone morphogenetic protein 4 in the formation of the node and primitive streak and coordination of left-right asymmetry in the mouse Development 129 2002 4685 4696
42. A. Nagy, J. Rossant, R. Nagy, W. Abramow-Newerly, and J.C. Roder Derivation of completely cell culture-derived mice from early-passage embryonic stem cells Proc Natl Acad Sci USA 90 1993 8424 8428
43. H. Zhang, and A. Bradley Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development Development 122 1996 2977 2986
44. Y. Mishina, A. Suzuki, N. Ueno, and R.R. Behringer Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis Genes Dev 9 1995 3027 3037
45. Y. Mishina, M.C. Hanks, S. Miura, M.D. Tallquist, and R.R. Behringer Generation of Bmpr/Alk3 conditional knockout mice Genesis 32 2002 69 72
46. M.D. Tallquist, and P. Soriano Epiblast-restricted Cre expression in MORE mice: a tool to distinguish embryonic vs. extra-embryonic gene function Genesis 26 2000 113 115
47. S. Davis, S. Miura, C. Hill, Y. Mishina, and J. Klingensmith BMP receptor IA is required in the mammalian embryo for endodermal morphogenesis and ectodermal patterning Dev Biol 270 2004 47 63
48. X. Qi, T.G. Li, and J. Hao BMP4 supports self-renewal of embryonic stem cells by inhibiting mitogen-activated protein kinase pathways Proc Natl Acad Sci USA 101 2004 6027 6032
49. Q.L. Ying, J. Nichols, I. Chambers, and A. Smith BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3 Cell 115 2003 281 292
50. Z. Gu, E.M. Reynolds, and J. Song The type I serine/threonine kinase receptor ActRIA (ALK2) is required for gastrulation of the mouse embryo Development 126 1999 2551 2561
51. B.A. Roelen, H.Y. Lin, V. Knezevic, E. Freund, and C.L. Mummery Expression of TGF-beta s and their receptors during implantation and organogenesis of the mouse embryo Dev Biol 166 1994 716 728
52. S.I. Yoshikawa, S. Aota, Y. Shirayoshi, and K. Okazaki The ActR-I activin receptor protein is expressed in notochord, lens placode and pituitary primordium cells in the mouse embryo Mech Dev 91 2000 439 444
53. S. Kishigami, S. Yoshikawa, T. Castranio, K. Okazaki, Y. Furuta, and Y. Mishina BMP signaling through ACVRI is required for left-right patterning in the early mouse embryo Dev Biol 276 2004 185 193
54. Y. Mishina, R. Crombie, A. Bradley, and R.R. Behringer Multiple roles for activin-like kinase-2 signaling during mouse embryogenesis Dev Biol 213 1999 314 326
55. S.M. de Sousa Lopes, B.A. Roelen, and R.M. Monteiro BMP signaling mediated by ALK2 in the visceral endoderm is necessary for the generation of primordial germ cells in the mouse embryo Genes Dev 18 2004 1838 1849
56. Y. Ying, X. Qi, and G.Q. Zhao Induction of primordial germ cells from murine epiblasts by synergistic action of BMP4 and BMP8B signaling pathways Proc Natl Acad Sci USA 98 2001 7858 7862
57. V. Kaartinen, and A. Nagy Removal of the floxed neo gene from a conditional knockout allele by the adenoviral Cre recombinase in vivo Genesis 31 2001 126 129
58. H. Beppu, M. Kawabata, and T. Hamamoto BMP type II receptor is required for gastrulation and early development of mouse embryos Dev Biol 221 2000 249 258
59. K.D. Tremblay, N.R. Dunn, and E.J. Robertson Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation Development 128 2001 3609 3621
60. R.J. Lechleider, J.L. Ryan, and L. Garrett Targeted mutagenesis of Smad1 reveals an essential role in chorioallantoic fusion Dev Biol 240 2001 157 167
61. E. Reissmann, H. Jornvall, and A. Blokzijl The orphan receptor ALK7 and the Activin receptor ALK4 mediate signaling by Nodal proteins during vertebrate development Genes Dev 15 2001 2010 2022
62. X. Zhou, H. Sasaki, L. Lowe, B.L. Hogan, and M.R. Kuehn Nodal is a novel TGF-beta-like gene expressed in the mouse node during gastrulation Nature 361 1993 543 547
63. F.L. Conlon, K.M. Lyons, and N. Takaesu A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse Development 120 1994 1919 1928
64. J. Brennan, C.C. Lu, D.P. Norris, T.A. Rodriguez, R.S. Beddington, and E.J. Robertson Nodal signalling in the epiblast patterns the early mouse embryo Nature 411 2001 965 969
65. D.P. Norris, and E.J. Robertson Asymmetric and node-specific nodal expression patterns are controlled by two distinct cis-acting regulatory elements Genes Dev 13 1999 1575 1588
66. I. Varlet, J. Collignon, and E.J. Robertson nodal expression in the primitive endoderm is required for specification of the anterior axis during mouse gastrulation Development 124 1997 1033 1044
67. C. Meno, K. Gritsman, and S. Ohishi Mouse Lefty2 and zebrafish antivin are feedback inhibitors of nodal signaling during vertebrate gastrulation Mol Cell 4 1999 287 298
68. A. Perea-Gomez, F.D. Vella, and W. Shawlot Nodal antagonists in the anterior visceral endoderm prevent the formation of multiple primitive streaks Dev Cell 3 2002 745 756
69. M. Yamamoto, Y. Saijoh, and A. Perea-Gomez Nodal antagonists regulate formation of the anteroposterior axis of the mouse embryo Nature 428 2004 387 392
70. Y. Furuta, and B.L. Hogan BMP4 is essential for lens induction in the mouse embryo Genes Dev 12 1998 3764 3775
71. T. Fujiwara, N.R. Dunn, and B.L. Hogan Bone morphogenetic protein 4 in the extraembryonic mesoderm is required for allantois development and the localization and survival of primordial germ cells in the mouse Proc Natl Acad Sci USA 98 2001 13739 13744
72. W. Shawlot, M. Wakamiya, K.M. Kwan, A. Kania, T.M. Jessell, and R.R. Behringer Lim1 is required in both primitive streak-derived tissues and visceral endoderm for head formation in the mouse Development 126 1999 4925 4932
73. N. Dewulf, K. Verschueren, and O. Lonnoy Distinct spatial and temporal expression patterns of two type I receptors for bone morphogenetic proteins during mouse embryogenesis Endocrinology 136 1995 2652 3663
74. S.T. Baur, J.J. Mai, and S.M. Dymecki Combinatorial signaling through BMP receptor IB and GDF5: shaping of the distal mouse limb and the genetics of distal limb diversity Development 127 2000 605 619
75. S.E. Yi, A. Daluiski, R. Pederson, V. Rosen, and K.M. Lyons The type I BMP receptor BMPRIB is required for chondrogenesis in the mouse limb Development 127 2000 621 630
76. D.P. Norris, J. Brennan, E.K. Bikoff, and E.J. Robertson The Foxh1-dependent autoregulatory enhancer controls the level of Nodal signals in the mouse embryo Development 129 2002 3455 3468
77. C.C. Lu, and E.J. Robertson Multiple roles for Nodal in the epiblast of the mouse embryo in the establishment of anterior-posterior patterning Dev Biol 273 2004 149 159
78. M. Nomura, and E. Li Smad2 role in mesoderm formation, left-right patterning and craniofacial development Nature 393 1998 786 790
79. W.R. Waldrip, E.K. Bikoff, P.A. Hoodless, J.L. Wrana, and E.J. Robertson Smad2 signaling in extraembryonic tissues determines anterior-posterior polarity of the early mouse embryo Cell 92 1998 797 808
80. K.D. Tremblay, P.A. Hoodless, E.K. Bikoff, and E.J. Robertson Formation of the definitive endoderm in mouse is a Smad2-dependent process Development 127 2000 3079 3090
81. S.D. Vincent, N.R. Dunn, S. Hayashi, D.P. Norris, and E.J. Robertson Cell fate decisions within the mouse organizer are governed by graded Nodal signals Genes Dev 17 2003 1646 1662
82. Y. Zhu, J.A. Richardson, L.F. Parada, and J.M. Graff Smad3 mutant mice develop metastatic colorectal cancer Cell 94 1998 703 714
83. M.B. Datto, J.P. Frederick, L. Pan, A.J. Borton, Y. Zhuang, and X.F. Wang Targeted disruption of Smad3 reveals an essential role in transforming growth factor beta-mediated signal transduction Mol Cell Biol 19 1999 2495 2504
84. X. Yang, J.J. Letterio, and R.J. Lechleider Targeted disruption of SMAD3 results in impaired mucosal immunity and diminished T cell responsiveness to TGF-beta EMBO J 18 1999 1280 1291
85. N.R. Dunn, S.D. Vincent, L. Oxburgh, E.J. Robertson, and E.K. Bikoff Combinatorial activities of Smad2 and Smad3 regulate mesoderm formation and patterning in the mouse embryo Development 131 2004 1717 1728
86. C. Sirard, J.L. de la Pompa, and A. Elia The tumor suppressor gene Smad4/Dpc4 is required for gastrulation and later for anterior development of the mouse embryo Genes Dev 12 1998 107 119
87. X. Yang, C. Li, X. Xu, and C. Deng The tumor suppressor SMAD4/DPC4 is essential for epiblast proliferation and mesoderm induction in mice Proc Natl Acad Sci USA 95 1998 3667 3672
88. G.C. Chu, N.R. Dunn, D.C. Anderson, L. Oxburgh, and E.J. Robertson Differential requirements for Smad4 in TGFbeta-dependent patterning of the early mouse embryo Development 131 2004 3501 3512
89. H. Hamada, C. Meno, D. Watanabe, and Y. Saijoh Establishment of vertebrate left-right asymmetry Nat Rev Genet 3 2002 103 113
90. E.N. Meyers, and G.R. Martin Differences in left-right axis pathways in mouse and chick: functions of FGF8 and SHH Science 285 1999 403 406
91. C.V. Wright Mechanisms of left-right asymmetry: what's right and what's left? Dev Cell 1 2001 179 186
92. J. Capdevila, K.J. Vogan, C.J. Tabin, and J.C. Izpisua Belmonte Mechanisms of left-right determination in vertebrates Cell 101 2000 9 21
93. A.R. Palmer Symmetry breaking and the evolution of development Science 306 2004 828 833
94. M. Logan, S.M. Pagan-Westphal, D.M. Smith, L. Paganessi, and C.J. Tabin The transcription factor Pitx2 mediates situs-specific morphogenesis in response to left-right asymmetric signals Cell 94 1998 307 317
95. M.E. Piedra, J.M. Icardo, M. Albajar, J.C. Rodriguez-Rey, and M.A. Ros Pitx2 participates in the late phase of the pathway controlling left-right asymmetry Cell 94 1998 319 324
96. H. Yoshioka, C. Meno, and K. Koshiba Pitx2, a bicoid-type homeobox gene, is involved in a lefty-signaling pathway in determination of left-right asymmetry Cell 94 1998 299 305
97. M. Fujinaga Development of sidedness of asymmetric body structures in vertebrates Int J Dev Biol 41 1997 153 186
98. S. Nonaka, Y. Tanaka, and Y. Okada Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein Cell 95 1998 829 837
99. J.J. Essner, K.J. Vogan, M.K. Wagner, C.J. Tabin, H.J. Yost, and M. Brueckner Conserved function for embryonic nodal cilia Nature 418 2002 37 38
100. Y. Okada, S. Nonaka, Y. Tanaka, Y. Saijoh, H. Hamada, and N. Hirokawa Abnormal nodal flow precedes situs inversus in iv and inv mice Mol Cell 4 1999 459 468
101. S. Nonaka, H. Shiratori, Y. Saijoh, and H. Hamada Determination of left-right patterning of the mouse embryo by artificial nodal flow Nature 418 2002 96 99
102. J. Collignon, I. Varlet, and E.J. Robertson Relationship between asymmetric nodal expression and the direction of embryonic turning Nature 381 1996 155 158
103. L.A. Lowe, D.M. Supp, and K. Sampath Conserved left-right asymmetry of nodal expression and alterations in murine situs inversus Nature 381 1996 158 161
104. L.A. Lowe, S. Yamada, and M.R. Kuehn Genetic dissection of nodal function in patterning the mouse embryo Development 128 2001 1831 1843
105. J. Brennan, D.P. Norris, and E.J. Robertson Nodal activity in the node governs left-right asymmetry Genes Dev 16 2002 2339 2344
106. Y. Saijoh, S. Oki, S. Ohishi, and H. Hamada Left-right patterning of the mouse lateral plate requires nodal produced in the node Dev Biol 256 2003 160 172
107. S.P. Oh, and E. Li The signaling pathway mediated by the type IIB activin receptor controls axial patterning and lateral asymmetry in the mouse Genes Dev 11 1997 1812 1826
108. J. Song, S.P. Oh, and H. Schrewe The type II activin receptors are essential for egg cylinder growth, gastrulation, and rostral head development in mice Dev Biol 213 1999 157 169
109. S.P. Oh, and E. Li Gene-dosage-sensitive genetic interactions between inversus viscerum (iv), nodal, and activin type IIB receptor (ActRIIB) genes in asymmetrical patterning of the visceral organs along the left-right axis Dev Dyn 224 2002 279 290
110. A. Raya, and J.C. Belmonte Sequential transfer of left-right information during vertebrate embryo development Curr Opin Genet Dev 14 2004 575 581
111. C.T. Rankin, T. Bunton, A.M. Lawler, and S.J. Lee Regulation of left-right patterning in mice by growth/differentiation factor-1 Nat Genet 24 2000 262 265
112. N.A. Wall, E.J. Craig, P.A. Labosky, and D.S. Kessler Mesendoderm induction and reversal of left-right pattern by mouse Gdf1, a Vg1-related gene Dev Biol 227 2000 495 509
113. C. Yeo, and M. Whitman Nodal signals to Smads through cripto-dependent and cripto-independent mechanisms Mol Cell 7 2001 949 957
114. Y.T. Yan, K. Gritsman, and J. Ding Conserved requirement for EGF-CFC genes in vertebrate left-right axis formation Genes Dev 13 1999 2527 2537
115. U. Gaio, A. Schweickert, and A. Fischer A role of the cryptic gene in the correct establishment of the left-right axis Curr Biol 9 1999 1339 1342
116. C. Meno, A. Shimono, and Y. Saijoh lefty-1 is required for left-right determination as a regulator of lefty-2 and nodal Cell 94 1998 287 297
117. R. Sakuma, Y. Ohnishi Yi, and C. Meno Inhibition of Nodal signalling by Lefty mediated through interaction with common receptors and efficient diffusion Genes Cells 7 2002 401 412
118. M. Yamamoto, N. Mine, and K. Mochida Nodal signaling induces the midline barrier by activating Nodal expression in the lateral plate Development 130 2003 1795 1804
119. W.W. Branford, and H.J. Yost Nodal signaling: cryptic lefty mechanism of antagonism decoded Curr Biol 14 2004 341 343
120. C. Chen, and M.M. Shen Two modes by which Lefty proteins inhibit nodal signaling Curr Biol 14 2004 618 624
121. S.K. Cheng, F. Olale, A.H. Brivanlou, and A.F. Schier Lefty blocks a subset of TGFbeta signals by antagonizing EGF-CFC coreceptors PLoS Biol 2 2004 30
122. C. Meno, J. Takeuchi, and R. Sakuma Diffusion of nodal signaling activity in the absence of the feedback inhibitor Lefty2 Dev Cell 1 2001 127 138
123. C. Meno, Y. Ito, and Y. Saijoh Two closely-related left-right asymmetrically expressed genes, lefty-1 and lefty-2: their distinct expression domains, chromosomal linkage and direct neuralizing activity in Xenopus embryos Genes Cells 2 1997 513 524
124. W.W. Branford, J.J. Essner, and H.J. Yost Regulation of gut and heart left-right asymmetry by context-dependent interactions between Xenopus lefty and BMP4 signaling Dev Biol 223 2000 291 306
125. L. Ulloa, and S. Tabibzadeh Lefty inhibits receptor-regulated Smad phosphorylation induced by the activated transforming growth factor-beta receptor J Biol Chem 276 2001 21397 21404
126. A.F. Ramsdell, and H.J. Yost Cardiac looping and the vertebrate left-right axis: antagonism of left-sided Vg1 activity by a right-sided ALK2-dependent BMP pathway Development 126 1999 5195 5205
127. C. Rodriguez Esteban, J. Capdevila, A.N. Economides, J. Pascual, A. Ortiz, and J.C. Izpisua Belmonte The novel Cer-like protein Caronte mediates the establishment of embryonic left-right asymmetry Nature 401 1999 243 251
128. Y. Yokouchi, K.J. Vogan, R.V. Pearse 2nd, and C.J. Tabin Antagonistic signaling by Caronte, a novel Cerberus-related gene, establishes left-right asymmetric gene expression Cell 98 1999 573 583
129. M.E. Piedra, and M.A. Ros BMP signaling positively regulates Nodal expression during left right specification in the chick embryo Development 129 2002 3431 3440
130. T. Schlange, H.H. Arnold, and T. Brand BMP2 is a positive regulator of Nodal signaling during left-right axis formation in the chicken embryo Development 129 2002 3421 3429
131. H. Chang, A. Zwijsen, H. Vogel, D. Huylebroeck, and M.M. Matzuk Smad5 is essential for left-right asymmetry in mice Dev Biol 219 2000 71 78
132. T. Ebisawa, K. Tada, and I. Kitajima Characterization of bone morphogenetic protein-6 signaling pathways in osteoblast differentiation J Cell Sci 112 Pt 20 1999 3519 3527
133. M. Macias-Silva, P.A. Hoodless, S.J. Tang, M. Buchwald, and J.L. Wrana Specific activation of Smad1 signaling pathways by the BMP7 type I receptor, ALK2 J Biol Chem 273 1998 25628 25636
134. M.J. Solloway, and E.J. Robertson Early embryonic lethality in Bmp5; Bmp7 double mutant mice suggests functional redundancy within the 60A subgroup Development 126 1999 1753 1768
135. A.T. Dudley, K.M. Lyons, and E.J. Robertson A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye Genes Dev 9 1995 2795 2807
136. G. Luo, C. Hofmann, A.L. Bronckers, M. Sohocki, A. Bradley, and G. Karsenty BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning Genes Dev 9 1995 2808 2820
137. T. Tsukui, J. Capdevila, and K. Tamura Multiple left-right asymmetry defects in Shh(-/-) mutant mice unveil a convergence of the shh and retinoic acid pathways in the control of Lefty-1 Proc Natl Acad Sci USA 96 1999 11376 11381
138. X.M. Zhang, M. Ramalho-Santos, and A.P. McMahon Smoothened mutants reveal redundant roles for Shh and Ihh signaling including regulation of L/R symmetry by the mouse node Cell 106 2001 781 792
139. A. Monsoro-Burq, and N.M. Le Douarin BMP4 plays a key role in left-right patterning in chick embryos by maintaining Sonic Hedgehog asymmetry Mol Cell 7 2001 789 799
140. J.T. Thomas, K. Lin, M. Nandedkar, M. Camargo, J. Cervenka, and F.P. Luyten A human chondrodysplasia due to a mutation in a TGF-beta superfamily member Nat Genet 12 1996 315 317
141. J.T. Thomas, M.W. Kilpatrick, and K. Lin Disruption of human limb morphogenesis by a dominant negative mutation in CDMP1 Nat Genet 17 1997 58 64
142. D.W. Johnson, J.N. Berg, and M.A. Baldwin Mutations in the activin receptor-like kinase 1 gene in hereditary haemorrhagic telangiectasia type 2 Nat Genet 13 1996 189 195
143. K.B. Lane, R.D. Machado, and M.W. Pauciulo Heterozygous germline mutations in BMPR2, encoding a TGF-beta receptor, cause familial primary pulmonary hypertension. The International PPH Consortium Nat Genet 26 2000 81 84
144. X.P. Zhou, K. Woodford-Richens, and R. Lehtonen Germline mutations in BMPR1A/ALK3 cause a subset of cases of juvenile polyposis syndrome and of Cowden and Bannayan-Riley-Ruvalcaba syndromes Am J Hum Genet 69 2001 704 711
145. J.R. Howe, J.L. Bair, and M.G. Sayed Germline mutations of the gene encoding bone morphogenetic protein receptor 1A in juvenile polyposis Nat Genet 28 2001 184 187
146. S. Imbeaud, E. Faure, and I. Lamarre Insensitivity to anti-mullerian hormone due to a mutation in the human anti-mullerian hormone receptor Nat Genet 11 1995 382 388
147. M. Pashmforoush, J.T. Lu, and H. Chen Nkx2-5 pathways and congenital heart disease; loss of ventricular myocyte lineage specification leads to progressive cardiomyopathy and complete heart block Cell 117 2004 373 386
148. R.B. Rountree, M. Schoor, and H. Chen BMP receptor signaling is required for postnatal maintenance of articular cartilage PLoS Biol 2 2004 e355
149. Y. Mishina, M.W. Starbuck, and M.A. Gentile Bone morphogenetic protein type IA receptor signaling regulates postnatal osteoblast function and bone remodeling J Biol Chem 279 2004 27560 27566
150. S.P. Oh, T. Seki, and K.A. Goss Activin receptor-like kinase 1 modulates transforming growth factor-beta 1 signaling in the regulation of angiogenesis Proc Natl Acad Sci USA 97 2000 2626 2631
151. J. Zhang, C. Niu, and L. Ye Identification of the haematopoietic stem cell niche and control of the niche size Nature 425 2003 836 841
152. X.C. He, J. Zhang, and W.G. Tong BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-beta-catenin signaling Nat Genet 36 2004 1117 1121
153. S.P. Jamin, N.A. Arango, Y. Mishina, M.C. Hanks, and R.R. Behringer Requirement of Bmpr1a for Mullerian duct regression during male sexual development Nat Genet 32 2002 408 410
154. M. Yuhki, M. Yamada, and M. Kawano BMPR1A signaling is necessary for hair follicle cycling and hair shaft differentiation in mice Development 131 2004 1825 1833
155. T. Andl, K. Ahn, and A. Kairo Epithelial Bmpr1a regulates differentiation and proliferation in postnatal hair follicles and is essential for tooth development Development 131 2004 2257 2268
156. K. Ming Kwan, A.G. Li, X.J. Wang, W. Wurst, and R.R. Behringer Essential roles of BMPR-IA signaling in differentiation and growth of hair follicles and in skin tumorigenesis Genesis 39 2004 10 25
157. K. Kobielak, H.A. Pasolli, L. Alonso, L. Polak, and E. Fuchs Defining BMP functions in the hair follicle by conditional ablation of BMP receptor IA J Cell Biol 163 2003 609 623
158. V. Gaussin, T. Van de Putte, and Y. Mishina Endocardial cushion and myocardial defects after cardiac myocyte-specific conditional deletion of the bone morphogenetic protein receptor ALK3 Proc Natl Acad Sci USA 99 2002 2878 2883
159. K. Jiao, H. Kulessa, and K. Tompkins An essential role of Bmp4 in the atrioventricular septation of the mouse heart Genes Dev 17 2003 2362 2367
160. H. Oh, X. Chi, and S.B. Bradfute Cardiac muscle plasticity in adult and embryo by heart-derived progenitor cells Ann N Y Acad Sci 1015 2004 182 189
161. V. Kaartinen, M. Dudas, A. Nagy, S. Sridurongrit, M.M. Lu, and J.A. Epstein Cardiac outflow tract defects in mice lacking ALK2 in neural crest cells Development 131 2004 3481 3490
162. M. Dudas, S. Sridurongrit, A. Nagy, K. Okazaki, and V. Kaartinen Craniofacial defects in mice lacking BMP type I receptor Alk2 in neural crest cells Mech Dev 121 2004 173 182
163. H. Chen, S. Shi, and L. Acosta BMP10 is essential for maintaining cardiac growth during murine cardiogenesis Development 131 2004 2219 2231