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PMID: 15473842 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S. Review

Dorsal-ventral patterning and neural induction in Xenopus embryos.

Annual review of cell and developmental biology ·Vol. 20 ·2004-00-00 ·Pages 285-308

De Robertis EM, Kuroda H

Abstract

We review the current status of research in dorsal-ventral (D-V) patterning in vertebrates. Emphasis is placed on recent work on Xenopus, which provides a paradigm for vertebrate development based on a rich heritage of experimental embryology. D-V patterning starts much earlier than previously thought, under the influence of a dorsal nuclear -Catenin signal. At mid-blastula two signaling centers are present on the dorsal side: The prospective neuroectoderm expresses bone morphogenetic protein (BMP) antagonists, and the future dorsal endoderm secretes Nodal-related mesoderm-inducing factors. When dorsal mesoderm is formed at gastrula, a cocktail of growth factor antagonists is secreted by the Spemann organizer and further patterns the embryo. A ventral gastrula signaling center opposes the actions of the dorsal organizer, and another set of secreted antagonists is produced ventrally under the control of BMP4. The early dorsal -Catenin signal inhibits BMP expression at the transcriptional level and promotes expression of secreted BMP antagonists in the prospective central nervous system (CNS). In the absence of mesoderm, expression of Chordin and Noggin in ectoderm is required for anterior CNS formation. FGF (fibroblast growth factor) and IGF (insulin-like growth factor) signals are also potent neural inducers. Neural induction by anti-BMPs such as Chordin requires mitogen-activated protein kinase (MAPK) activation mediated by FGF and IGF. These multiple signals can be integrated at the level of Smad1. Phosphorylation by BMP receptor stimulates Smad1 transcriptional activity, whereas phosphorylation by MAPK has the opposite effect. Neural tissue is formed only at very low levels of activity of BMP-transducing Smads, which require the combination of both low BMP levels and high MAPK signals. Many of the molecular players that regulate D-V patterning via regulation of BMP signaling have been conserved between Drosophila and the vertebrates.

MeSH Terms
Animals Body Patterning/physiology Bone Morphogenetic Proteins/metabolism,physiology Central Nervous System/embryology Cytoskeletal Proteins/physiology Gastrula/physiology Signal Transduction/physiology Trans-Activators/physiology Vertebrates/embryology Xenopus/embryology Xenopus Proteins beta Catenin
Chemicals
Bone Morphogenetic Proteins CTNNB1 protein, Xenopus Cytoskeletal Proteins Trans-Activators Xenopus Proteins beta Catenin
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
De Robertis Edward M
Howard Hughes Medical Institute, Department of Biological Chemistry, University of California-Los Angeles, Los Angeles, CA 90095-1662, USA. [email protected]
Kuroda Hiroki
References (111)
111 references, click to expand
  1. The head inducer Cerberus is a multifunctional antagonist of Nodal, BMP and Wnt signals.
    Nature. 1999 Feb 25;397(6721):707-10 PMID: 10067895
  2. Neural induction. A bird's eye view.
    Trends Genet. 1999 Jan;15(1):20-4 PMID: 10087929
  3. Comparison of early nerve cord development in insects and vertebrates.
    Development. 1999 Jun;126(11):2309-25 PMID: 10225991
  4. The role of tolloid/mini fin in dorsoventral pattern formation of the zebrafish embryo.
    Development. 1999 Jun;126(14):3119-30 PMID: 10375503
  5. Establishment of the dorsal-ventral axis in Xenopus embryos coincides with the dorsal enrichment of dishevelled that is dependent on cortical rotation.
    J Cell Biol. 1999 Jul 26;146(2):427-37 PMID: 10427095
  6. Mammalian BMP-1/Tolloid-related metalloproteinases, including novel family member mammalian Tolloid-like 2, have differential enzymatic activities and distributions of expression relevant to patterning and skeletogenesis.
    Dev Biol. 1999 Sep 15;213(2):283-300 PMID: 10479448
  7. Silencing of TGF-beta signalling by the pseudoreceptor BAMBI.
    Nature. 1999 Sep 30;401(6752):480-5 PMID: 10519551
  8. Synexpression groups in eukaryotes.
    Nature. 1999 Dec 2;402(6761):483-7 PMID: 10591207
  9. Wnt signaling in Xenopus embryos inhibits bmp4 expression and activates neural development.
    Genes Dev. 1999 Dec 1;13(23):3149-59 PMID: 10601040
  10. Neural induction.
    Annu Rev Cell Dev Biol. 1999;15:411-33 PMID: 10611968
  11. Neural induction and patterning in the mouse in the absence of the node and its derivatives.
    Dev Biol. 1999 Dec 15;216(2):535-49 PMID: 10642791
  12. BMP-binding modules in chordin: a model for signalling regulation in the extracellular space.
    Development. 2000 Feb;127(4):821-30 PMID: 10648240
  13. Endodermal Nodal-related signals and mesoderm induction in Xenopus.
    Development. 2000 Mar;127(6):1173-83 PMID: 10683171
  14. The organizer factors Chordin and Noggin are required for mouse forebrain development.
    Nature. 2000 Feb 10;403(6770):658-61 PMID: 10688202
  15. Bmp4 and Fgf10 play opposing roles during lung bud morphogenesis.
    Development. 2000 Jun;127(12):2695-704 PMID: 10821767
  16. The evolutionarily conserved BMP-binding protein Twisted gastrulation promotes BMP signalling.
    Nature. 2000 Jun 15;405(6788):757-63 PMID: 10866189
  17. Neural induction.
    Curr Opin Genet Dev. 2000 Aug;10(4):357-62 PMID: 10889069
  18. Convergence of dorsal, dpp, and egfr signaling pathways subdivides the drosophila neuroectoderm into three dorsal-ventral columns.
    Dev Biol. 2000 Aug 15;224(2):362-72 PMID: 10926773
  19. 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 Sep;127(18):3947-59 PMID: 10952893
  20. A direct screen for secreted proteins in Xenopus embryos identifies distinct activities for the Wnt antagonists Crescent and Frzb-1.
    Mech Dev. 2000 Sep;96(2):183-95 PMID: 10960783
  21. LDL-receptor-related proteins in Wnt signal transduction.
    Nature. 2000 Sep 28;407(6803):530-5 PMID: 11029007
  22. The role of Xenopus dickkopf1 in prechordal plate specification and neural patterning.
    Development. 2000 Nov;127(22):4981-92 PMID: 11044411
  23. Functional interaction of vega2 and goosecoid homeobox genes in zebrafish.
    Genesis. 2000 Oct;28(2):58-67 PMID: 11064422
  24. Different activities of the frizzled-related proteins frzb2 and sizzled2 during Xenopus anteroposterior patterning.
    Dev Biol. 2000 Nov 1;227(1):118-32 PMID: 11076681
  25. Two novel nodal-related genes initiate early inductive events in Xenopus Nieuwkoop center.
    Development. 2000 Dec;127(24):5319-29 PMID: 11076754
  26. FGF-8 stimulates neuronal differentiation through FGFR-4a and interferes with mesoderm induction in Xenopus embryos.
    Curr Biol. 2000 Nov 30;10(23):1511-4 PMID: 11114518
  27. Head and trunk in zebrafish arise via coinhibition of BMP signaling by bozozok and chordino.
    Genes Dev. 2000 Dec 15;14(24):3087-92 PMID: 11124801
  28. The Spemann organizer and embryonic head induction.
    EMBO J. 2001 Feb 15;20(4):631-7 PMID: 11179208
  29. The establishment of Spemann's organizer and patterning of the vertebrate embryo.
    Nat Rev Genet. 2000 Dec;1(3):171-81 PMID: 11252746
  30. Homologues of Twisted gastrulation are extracellular cofactors in antagonism of BMP signalling.
    Nature. 2001 Mar 22;410(6827):475-8 PMID: 11260715
  31. Twisted gastrulation is a conserved extracellular BMP antagonist.
    Nature. 2001 Mar 22;410(6827):479-83 PMID: 11260716
  32. Twisted gastrulation can function as a BMP antagonist.
    Nature. 2001 Mar 22;410(6827):483-7 PMID: 11260717
  33. Induction of embryonic primordia by implantation of organizers from a different species. 1923.
    Int J Dev Biol. 2001;45(1):13-38 PMID: 11291841
  34. Neural induction in the absence of mesoderm: beta-catenin-dependent expression of secreted BMP antagonists at the blastula stage in Xenopus.
    Dev Biol. 2001 Jun 1;234(1):161-73 PMID: 11356027
  35. LDL-receptor-related protein 6 is a receptor for Dickkopf proteins.
    Nature. 2001 May 17;411(6835):321-5 PMID: 11357136
  36. Neural induction: toward a unifying mechanism.
    Nat Neurosci. 2001 Nov;4 Suppl:1161-8 PMID: 11687825
  37. Conservation and divergence in molecular mechanisms of axis formation.
    Annu Rev Genet. 2001;35:407-37 PMID: 11700289
  38. Dickkopf1 is required for embryonic head induction and limb morphogenesis in the mouse.
    Dev Cell. 2001 Sep;1(3):423-34 PMID: 11702953
  39. Neural and head induction by insulin-like growth factor signals.
    Dev Cell. 2001 Nov;1(5):655-65 PMID: 11709186
  40. Proteolytic cleavage of Chordin as a switch for the dual activities of Twisted gastrulation in BMP signaling.
    Development. 2001 Nov;128(22):4439-47 PMID: 11714670
  41. Beta-catenin, MAPK and Smad signaling during early Xenopus development.
    Development. 2002 Jan;129(1):37-52 PMID: 11782399
  42. The IGF pathway regulates head formation by inhibiting Wnt signaling in Xenopus.
    Dev Biol. 2002 Apr 15;244(2):407-17 PMID: 11944947
  43. Neural induction, the default model and embryonic stem cells.
    Nat Rev Neurosci. 2002 Apr;3(4):271-80 PMID: 11967557
  44. Chordin-like CR domains and the regulation of evolutionarily conserved extracellular signaling systems.
    Gene. 2002 Apr 3;287(1-2):39-47 PMID: 11992721
  45. The role of growth factors in tooth development.
    Int Rev Cytol. 2002;217:93-135 PMID: 12019566
  46. Kremen proteins are Dickkopf receptors that regulate Wnt/beta-catenin signalling.
    Nature. 2002 Jun 6;417(6889):664-7 PMID: 12050670
  47. Induction and initial patterning of the nervous system - the chick embryo enters the scene.
    Curr Opin Genet Dev. 2002 Aug;12(4):447-51 PMID: 12100891
  48. Robustness of the BMP morphogen gradient in Drosophila embryonic patterning.
    Nature. 2002 Sep 19;419(6904):304-8 PMID: 12239569
  49. Dorsoventral patterning in the zebrafish: bone morphogenetic proteins and beyond.
    Results Probl Cell Differ. 2002;40:72-95 PMID: 12353487
  50. The hypoblast of the chick embryo positions the primitive streak by antagonizing nodal signaling.
    Dev Cell. 2002 Nov;3(5):735-44 PMID: 12431379
  51. Nodal antagonists in the anterior visceral endoderm prevent the formation of multiple primitive streaks.
    Dev Cell. 2002 Nov;3(5):745-56 PMID: 12431380
  52. Functional gene screening in embryonic stem cells implicates Wnt antagonism in neural differentiation.
    Nat Biotechnol. 2002 Dec;20(12):1240-5 PMID: 12447396
  53. Xolloid-related: a novel BMP1/Tolloid-related metalloprotease is expressed during early Xenopus development.
    Mech Dev. 2002 Dec;119(2):177-90 PMID: 12464431
  54. Structural basis of BMP signalling inhibition by the cystine knot protein Noggin.
    Nature. 2002 Dec 12;420(6916):636-42 PMID: 12478285
  55. Early steps in the formation of neural tissue in ascidian embryos.
    Dev Biol. 2002 Dec 15;252(2):151-69 PMID: 12482707
  56. The secreted Frizzled-related protein Sizzled functions as a negative feedback regulator of extreme ventral mesoderm.
    Development. 2003 Feb;130(4):805-16 PMID: 12506010
  57. Chordin is required for the Spemann organizer transplantation phenomenon in Xenopus embryos.
    Dev Cell. 2003 Feb;4(2):219-30 PMID: 12586065
  58. Mammalian twisted gastrulation is essential for skeleto-lymphogenesis.
    Mol Cell Biol. 2003 Apr;23(8):2969-80 PMID: 12665593
  59. The BMP antagonist noggin regulates cranial suture fusion.
    Nature. 2003 Apr 10;422(6932):625-9 PMID: 12687003
  60. Ogon/Secreted Frizzled functions as a negative feedback regulator of Bmp signaling.
    Development. 2003 Jun;130(12):2705-16 PMID: 12736214
  61. Secreted antagonists of the Wnt signalling pathway.
    J Cell Sci. 2003 Jul 1;116(Pt 13):2627-34 PMID: 12775774
  62. Mechanisms of TGF-beta signaling from cell membrane to the nucleus.
    Cell. 2003 Jun 13;113(6):685-700 PMID: 12809600
  63. The role of chordin/Bmp signals in mammalian pharyngeal development and DiGeorge syndrome.
    Development. 2003 Aug;130(15):3567-78 PMID: 12810603
  64. bozozok directly represses bmp2b transcription and mediates the earliest dorsoventral asymmetry of bmp2b expression in zebrafish.
    Development. 2003 Aug;130(16):3639-49 PMID: 12835381
  65. The pro-BMP activity of Twisted gastrulation is independent of BMP binding.
    Development. 2003 Sep;130(17):4047-56 PMID: 12874126
  66. The molecular nature of the zebrafish tail organizer.
    Nature. 2003 Jul 24;424(6947):448-52 PMID: 12879074
  67. The ventralized ogon mutant phenotype is caused by a mutation in the zebrafish homologue of Sizzled, a secreted Frizzled-related protein.
    Dev Biol. 2003 Aug 1;260(1):58-67 PMID: 12885555
  68. BMPER, a novel endothelial cell precursor-derived protein, antagonizes bone morphogenetic protein signaling and endothelial cell differentiation.
    Mol Cell Biol. 2003 Aug;23(16):5664-79 PMID: 12897139
  69. Dkk1 and noggin cooperate in mammalian head induction.
    Genes Dev. 2003 Sep 15;17(18):2239-44 PMID: 12952897
  70. Twisted gastrulation loss-of-function analyses support its role as a BMP inhibitor during early Xenopus embryogenesis.
    Development. 2003 Oct;130(20):4975-88 PMID: 12952901
  71. Evidence for antagonism of BMP-4 signals by MAP kinase during Xenopus axis determination and neural specification.
    Differentiation. 2003 Sep;71(7):434-44 PMID: 12969336
  72. CHRD, a novel domain in the BMP inhibitor chordin, is also found in microbial proteins.
    Trends Biochem Sci. 2003 Sep;28(9):470-3 PMID: 13678956
  73. GBP binds kinesin light chain and translocates during cortical rotation in Xenopus eggs.
    Development. 2003 Nov;130(22):5425-36 PMID: 14507779
  74. Mouse Crossveinless-2 is the vertebrate homolog of a Drosophila extracellular regulator of BMP signaling.
    Mech Dev. 2002 Dec;119 Suppl 1:S179-84 PMID: 14516682
  75. Comparative genomic analysis of the eight-membered ring cystine knot-containing bone morphogenetic protein antagonists.
    Mol Endocrinol. 2004 Jan;18(1):1-12 PMID: 14525956
  76. Inactivation of mouse Twisted gastrulation reveals its role in promoting Bmp4 activity during forebrain development.
    Development. 2004 Jan;131(2):413-24 PMID: 14681194
  77. Xenopus tropicalis nodal-related gene 3 regulates BMP signaling: an essential role for the pro-region.
    Dev Biol. 2004 Jan 1;265(1):155-68 PMID: 14697360
  78. Integration of Smad and MAPK pathways: a link and a linker revisited.
    Genes Dev. 2003 Dec 15;17(24):2993-7 PMID: 14701870
  79. Integration of IGF, FGF, and anti-BMP signals via Smad1 phosphorylation in neural induction.
    Genes Dev. 2003 Dec 15;17(24):3023-8 PMID: 14701872
  80. A mechanism for Wnt coreceptor activation.
    Mol Cell. 2004 Jan 16;13(1):149-56 PMID: 14731402
  81. Human Crossveinless-2 is a novel inhibitor of bone morphogenetic proteins.
    Biochem Biophys Res Commun. 2004 Mar 5;315(2):272-80 PMID: 14766204
  82. Nodal antagonists regulate formation of the anteroposterior axis of the mouse embryo.
    Nature. 2004 Mar 25;428(6981):387-92 PMID: 15004567
  83. The mammalian twisted gastrulation gene functions in foregut and craniofacial development.
    Dev Biol. 2004 Mar 15;267(2):374-86 PMID: 15013800
  84. Analysis of Spemann organizer formation in Xenopus embryos by cDNA macroarrays.
    Dev Biol. 2004 May 15;269(2):552-66 PMID: 15110719
  85. Neural induction in Xenopus: requirement for ectodermal and endomesodermal signals via Chordin, Noggin, beta-Catenin, and Cerberus.
    PLoS Biol. 2004 May;2(5):E92 PMID: 15138495
  86. In vivo convergence of BMP and MAPK signaling pathways: impact of differential Smad1 phosphorylation on development and homeostasis.
    Genes Dev. 2004 Jun 15;18(12):1482-94 PMID: 15198985
  87. Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid.
    Cell. 1991 Dec 20;67(6):1111-20 PMID: 1684739
  88. A homeobox-containing marker of posterior neural differentiation shows the importance of predetermination in neural induction.
    Cell. 1987 Aug 28;50(5):749-58 PMID: 2441873
  89. Wilhelm Roux Arch Entwickl Mech Org. 1933 Dec;129(4):669-793 PMID: 28353925
  90. Wilhelm Roux Arch Entwickl Mech Org. 1925 Dec;106(1-4):503-541 PMID: 28354330
  91. Expression of Epi 1, an epidermis-specific marker in Xenopus laevis embryos, is specified prior to gastrulation.
    Dev Biol. 1988 Oct;129(2):380-9 PMID: 3166428
  92. Induction of epidermis and inhibition of neural fate by Bmp-4.
    Nature. 1995 Jul 27;376(6538):331-3 PMID: 7630398
  93. The ventral and posterior expression of the zebrafish homeobox gene eve1 is perturbed in dorsalized and mutant embryos.
    Development. 1993 Dec;119(4):1261-75 PMID: 7905819
  94. On the function of BMP-4 in patterning the marginal zone of the Xenopus embryo.
    EMBO J. 1994 Nov 1;13(21):5015-25 PMID: 7957067
  95. FGF-4 and BMP-2 have opposite effects on limb growth.
    Nature. 1993 Jan 7;361(6407):68-71 PMID: 8421496
  96. Antagonizing the Spemann organizer: role of the homeobox gene Xvent-1.
    EMBO J. 1995 Dec 15;14(24):6268-79 PMID: 8557046
  97. A common plan for dorsoventral patterning in Bilateria.
    Nature. 1996 Mar 7;380(6569):37-40 PMID: 8598900
  98. Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4.
    Cell. 1996 Aug 23;86(4):589-98 PMID: 8752213
  99. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4.
    Cell. 1996 Aug 23;86(4):599-606 PMID: 8752214
  100. Cerberus is a head-inducing secreted factor expressed in the anterior endoderm of Spemann's organizer.
    Nature. 1996 Aug 15;382(6592):595-601 PMID: 8757128
  101. Beta-catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos.
    Mech Dev. 1996 Jul;57(2):191-8 PMID: 8843396
  102. Direct neural induction and selective inhibition of mesoderm and epidermis inducers by Xnr3.
    Development. 1997 Jan;124(2):483-92 PMID: 9053324
  103. Frzb-1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer.
    Cell. 1997 Mar 21;88(6):747-56 PMID: 9118218
  104. The zebrafish organizer requires chordino.
    Nature. 1997 Jun 26;387(6636):862-3 PMID: 9202118
  105. Head induction by simultaneous repression of Bmp and Wnt signalling in Xenopus.
    Nature. 1997 Oct 2;389(6650):517-9 PMID: 9333244
  106. Opposing BMP and EGF signalling pathways converge on the TGF-beta family mediator Smad1.
    Nature. 1997 Oct 9;389(6651):618-22 PMID: 9335504
  107. Sizzled: a secreted Xwnt8 antagonist expressed in the ventral marginal zone of Xenopus embryos.
    Development. 1997 Dec;124(23):4739-48 PMID: 9428410
  108. Formation and function of Spemann's organizer.
    Annu Rev Cell Dev Biol. 1997;13:611-67 PMID: 9442883
  109. Dickkopf-1 is a member of a new family of secreted proteins and functions in head induction.
    Nature. 1998 Jan 22;391(6665):357-62 PMID: 9450748
  110. Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite.
    Genes Dev. 1998 May 15;12(10):1438-52 PMID: 9585504
  111. Axis development and early asymmetry in mammals.
    Cell. 1999 Jan 22;96(2):195-209 PMID: 9988215
Article Info
Journal
Annual review of cell and developmental biology
Abbr.
Annu Rev Cell Dev Biol
ISSN
1081-0706
Published
2004-00-00
Pages
285-308
Language
English
Region
United States
NLM ID
9600627
PMCID
PMC2280069
Subset
IM
Grants
NICHD NIH HHS · R37 HD021502 · United States
NICHD NIH HHS · R37 HD021502-18 · United States
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