Home LiteratureArticle Details
PMID: 11252746 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S. Review

The establishment of Spemann's organizer and patterning of the vertebrate embryo.

Nature reviews. Genetics ·Vol. 1 ·No. 3 ·2000-12-00 ·Pages 171-81

De Robertis EM, Larraín J, Oelgeschläger M, Wessely O

Abstract

Molecular studies have begun to unravel the sequential cell-cell signalling events that establish the dorsal-ventral, or 'back-to-belly', axis of vertebrate animals. In Xenopus and zebrafish, these events start with the movement of membrane vesicles associated with dorsal determinants. This mediates the induction of mesoderm by generating gradients of growth factors. Dorsal mesoderm then becomes a signalling centre, the Spemann's organizer, which secretes several antagonists of growth-factor signalling. Recent studies have led to new models for the regulation of cell-cell signalling during development, which may also apply to the homeostasis of adult tissues.

MeSH Terms
Amino Acid Sequence Animals Body Patterning Glycoproteins/chemistry,genetics Intercellular Signaling Peptides and Proteins Molecular Sequence Data Sequence Homology, Amino Acid Vertebrates/embryology
Chemicals
Glycoproteins Intercellular Signaling Peptides and Proteins chordin
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
De Robertis E M
Howard Hughes Medical Institute, and Department of Biological Chemistry, University of California, Los Angeles, California 90095-1662, USA. [email protected]
Larraín J
Oelgeschläger M
Wessely O
References (107)
107 references, click to expand
  1. Cleavage of Chordin by Xolloid metalloprotease suggests a role for proteolytic processing in the regulation of Spemann organizer activity.
    Cell. 1997 Oct 31;91(3):407-16 PMID: 9363949
  2. Production of a DPP activity gradient in the early Drosophila embryo through the opposing actions of the SOG and TLD proteins.
    Cell. 1997 Oct 31;91(3):417-26 PMID: 9363950
  3. Patterning the Xenopus blastula.
    Development. 1997 Nov;124(21):4179-91 PMID: 9334267
  4. Animal and vegetal pole cells of early Xenopus embryos respond differently to maternal dorsal determinants: implications for the patterning of the organiser.
    Development. 1997 Nov;124(21):4275-86 PMID: 9334276
  5. Siamois is required for formation of Spemann's organizer.
    Proc Natl Acad Sci U S A. 1997 Nov 25;94(24):13017-22 PMID: 9371792
  6. The molecular nature of zebrafish swirl: BMP2 function is essential during early dorsoventral patterning.
    Development. 1997 Nov;124(22):4457-66 PMID: 9409664
  7. Sizzled: a secreted Xwnt8 antagonist expressed in the ventral marginal zone of Xenopus embryos.
    Development. 1997 Dec;124(23):4739-48 PMID: 9428410
  8. The Xenopus homeobox gene twin mediates Wnt induction of goosecoid in establishment of Spemann's organizer.
    Development. 1997 Dec;124(23):4905-16 PMID: 9428427
  9. Formation and function of Spemann's organizer.
    Annu Rev Cell Dev Biol. 1997;13:611-67 PMID: 9442883
  10. 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
  11. Mixer, a homeobox gene required for endoderm development.
    Science. 1998 Jul 3;281(5373):91-6 PMID: 9651252
  12. Direct binding of follistatin to a complex of bone-morphogenetic protein and its receptor inhibits ventral and epidermal cell fates in early Xenopus embryo.
    Proc Natl Acad Sci U S A. 1998 Aug 4;95(16):9337-42 PMID: 9689081
  13. The smad5 mutation somitabun blocks Bmp2b signaling during early dorsoventral patterning of the zebrafish embryo.
    Development. 1999 May;126(10):2149-59 PMID: 10207140
  14. Removal of vegetal yolk causes dorsal deficencies and impairs dorsal-inducing ability of the yolk cell in zebrafish.
    Mech Dev. 1999 Mar;81(1-2):51-63 PMID: 10330484
  15. The role of tolloid/mini fin in dorsoventral pattern formation of the zebrafish embryo.
    Development. 1999 Jun;126(14):3119-30 PMID: 10375503
  16. Regulation of dorsal gene expression in Xenopus by the ventralizing homeodomain gene Vox.
    Dev Biol. 1999 Jul 15;211(2):293-305 PMID: 10395789
  17. 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
  18. Requirement for Wnt3 in vertebrate axis formation.
    Nat Genet. 1999 Aug;22(4):361-5 PMID: 10431240
  19. A two-step model for the fate determination of presumptive endodermal blastomeres in Xenopus embryos.
    Curr Biol. 1999 Aug 26;9(16):869-79 PMID: 10469589
  20. 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
  21. Mouse Lefty2 and zebrafish antivin are feedback inhibitors of nodal signaling during vertebrate gastrulation.
    Mol Cell. 1999 Sep;4(3):287-98 PMID: 10518210
  22. Signals from the yolk cell induce mesoderm, neuroectoderm, the trunk organizer, and the notochord in zebrafish.
    Dev Biol. 1999 Nov 15;215(2):167-81 PMID: 10545228
  23. The nieuwkoid/dharma homeobox gene is essential for bmp2b repression in the zebrafish pregastrula.
    Dev Biol. 1999 Nov 15;215(2):190-207 PMID: 10545230
  24. Mesoderm induction in Xenopus is a zygotic event regulated by maternal VegT via TGFbeta growth factors.
    Development. 1999 Dec;126(24):5759-70 PMID: 10572051
  25. Patterning the zebrafish axial skeleton requires early chordin function.
    Nat Genet. 1999 Dec;23(4):442-6 PMID: 10581032
  26. Synexpression groups in eukaryotes.
    Nature. 1999 Dec 2;402(6761):483-7 PMID: 10591207
  27. Wnt signaling in Xenopus embryos inhibits bmp4 expression and activates neural development.
    Genes Dev. 1999 Dec 1;13(23):3149-59 PMID: 10601040
  28. CRIM1, a novel gene encoding a cysteine-rich repeat protein, is developmentally regulated and implicated in vertebrate CNS development and organogenesis.
    Mech Dev. 2000 Feb;90(2):181-93 PMID: 10642437
  29. BMP-binding modules in chordin: a model for signalling regulation in the extracellular space.
    Development. 2000 Feb;127(4):821-30 PMID: 10648240
  30. Nodal signalling in vertebrate development.
    Nature. 2000 Jan 27;403(6768):385-9 PMID: 10667782
  31. Equivalent genetic roles for bmp7/snailhouse and bmp2b/swirl in dorsoventral pattern formation.
    Development. 2000 Mar;127(5):957-67 PMID: 10662635
  32. The lefty-related factor Xatv acts as a feedback inhibitor of nodal signaling in mesoderm induction and L-R axis development in xenopus.
    Development. 2000 Mar;127(5):1049-61 PMID: 10662644
  33. Requirement for beta-catenin in anterior-posterior axis formation in mice.
    J Cell Biol. 2000 Feb 7;148(3):567-78 PMID: 10662781
  34. Endodermal Nodal-related signals and mesoderm induction in Xenopus.
    Development. 2000 Mar;127(6):1173-83 PMID: 10683171
  35. The organizer factors Chordin and Noggin are required for mouse forebrain development.
    Nature. 2000 Feb 10;403(6770):658-61 PMID: 10688202
  36. Interaction between Wnt and TGF-beta signalling pathways during formation of Spemann's organizer.
    Nature. 2000 Feb 17;403(6771):781-5 PMID: 10693808
  37. Homeodomain and winged-helix transcription factors recruit activated Smads to distinct promoter elements via a common Smad interaction motif.
    Genes Dev. 2000 Feb 15;14(4):435-51 PMID: 10691736
  38. Regulation of early expression of Dlx3, a Xenopus anti-neural factor, by beta-catenin signaling.
    Mech Dev. 2000 Mar 1;91(1-2):227-35 PMID: 10704847
  39. Cooperative roles of Bozozok/Dharma and Nodal-related proteins in the formation of the dorsal organizer in zebrafish.
    Mech Dev. 2000 Mar 1;91(1-2):293-303 PMID: 10704853
  40. The putative wnt receptor Xenopus frizzled-7 functions upstream of beta-catenin in vertebrate dorsoventral mesoderm patterning.
    Development. 2000 May;127(9):1981-90 PMID: 10751186
  41. Processing of the Drosophila Sog protein creates a novel BMP inhibitory activity.
    Development. 2000 May;127(10):2143-54 PMID: 10769238
  42. Left-right asymmetric expression of the TGF beta-family member lefty in mouse embryos.
    Nature. 1996 May 9;381(6578):151-5 PMID: 8610011
  43. A molecular mechanism for the effect of lithium on development.
    Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8455-9 PMID: 8710892
  44. Smads and early developmental signaling by the TGFbeta superfamily.
    Genes Dev. 1998 Aug 15;12(16):2445-62 PMID: 9716398
  45. From cortical rotation to organizer gene expression: toward a molecular explanation of axis specification in Xenopus.
    Bioessays. 1998 Jul;20(7):536-45 PMID: 9723002
  46. The role of maternal VegT in establishing the primary germ layers in Xenopus embryos.
    Cell. 1998 Aug 21;94(4):515-24 PMID: 9727494
  47. Zebrafish organizer development and germ-layer formation require nodal-related signals.
    Nature. 1998 Sep 10;395(6698):181-5 PMID: 9744277
  48. Spatially restricted activation of the SAX receptor by SCW modulates DPP/TKV signaling in Drosophila dorsal-ventral patterning.
    Cell. 1998 Nov 13;95(4):483-94 PMID: 9827801
  49. Interpretation of a BMP activity gradient in Drosophila embryos depends on synergistic signaling by two type I receptors, SAX and TKV.
    Cell. 1998 Nov 13;95(4):495-506 PMID: 9827802
  50. Antivin, a novel and divergent member of the TGFbeta superfamily, negatively regulates mesoderm induction.
    Development. 1999 Jan;126(2):229-40 PMID: 9847237
  51. Mechanisms of Wnt signaling in development.
    Annu Rev Cell Dev Biol. 1998;14:59-88 PMID: 9891778
  52. The head inducer Cerberus is a multifunctional antagonist of Nodal, BMP and Wnt signals.
    Nature. 1999 Feb 25;397(6721):707-10 PMID: 10067895
  53. Type IIA procollagen containing the cysteine-rich amino propeptide is deposited in the extracellular matrix of prechondrogenic tissue and binds to TGF-beta1 and BMP-2.
    J Cell Biol. 1999 Mar 8;144(5):1069-80 PMID: 10085302
  54. Local inhibition and long-range enhancement of Dpp signal transduction by Sog.
    Nature. 1999 Apr 1;398(6726):427-31 PMID: 10201373
  55. A mouse cerberus/Dan-related gene family.
    Dev Biol. 1999 May 1;209(1):98-110 PMID: 10208746
  56. 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
  57. XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos.
    Cell. 1996 Aug 9;86(3):391-9 PMID: 8756721
  58. 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
  59. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4.
    Cell. 1996 Aug 23;86(4):599-606 PMID: 8752214
  60. The Xenopus dorsalizing factor noggin ventralizes Drosophila embryos by preventing DPP from activating its receptor.
    Cell. 1996 Aug 23;86(4):607-17 PMID: 8752215
  61. Genetic analysis of dorsoventral pattern formation in the zebrafish: requirement of a BMP-like ventralizing activity and its dorsal repressor.
    Genes Dev. 1996 Oct 1;10(19):2452-61 PMID: 8843197
  62. Beta-catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos.
    Mech Dev. 1996 Jul;57(2):191-8 PMID: 8843396
  63. Maternal beta-catenin establishes a 'dorsal signal' in early Xenopus embryos.
    Development. 1996 Oct;122(10):2987-96 PMID: 8898213
  64. The Xvent-2 homeobox gene is part of the BMP-4 signalling pathway controlling [correction of controling] dorsoventral patterning of Xenopus mesoderm.
    Development. 1996 Oct;122(10):3045-53 PMID: 8898218
  65. Expression of a dominant-negative Wnt blocks induction of MyoD in Xenopus embryos.
    Genes Dev. 1996 Nov 1;10(21):2805-17 PMID: 8946920
  66. Activation of Siamois by the Wnt pathway.
    Dev Biol. 1996 Nov 25;180(1):344-7 PMID: 8948596
  67. Direct neural induction and selective inhibition of mesoderm and epidermis inducers by Xnr3.
    Development. 1997 Jan;124(2):483-92 PMID: 9053324
  68. The homeobox gene bozozok promotes anterior neuroectoderm formation in zebrafish through negative regulation of BMP2/4 and Wnt pathways.
    Development. 2000 Jun;127(11):2333-45 PMID: 10804176
  69. Xenopus kielin: A dorsalizing factor containing multiple chordin-type repeats secreted from the embryonic midline.
    Proc Natl Acad Sci U S A. 2000 May 9;97(10):5291-6 PMID: 10779551
  70. bozozok and squint act in parallel to specify dorsal mesoderm and anterior neuroectoderm in zebrafish.
    Development. 2000 Jun;127(12):2583-92 PMID: 10821757
  71. Endogenous patterns of TGFbeta superfamily signaling during early Xenopus development.
    Development. 2000 Jul;127(13):2917-31 PMID: 10851136
  72. The evolutionarily conserved BMP-binding protein Twisted gastrulation promotes BMP signalling.
    Nature. 2000 Jun 15;405(6788):757-63 PMID: 10866189
  73. Beta-catenin signaling activity dissected in the early Xenopus embryo: a novel antisense approach.
    Dev Biol. 2000 Jun 1;222(1):124-34 PMID: 10885751
  74. Association of Smads with lymphoid enhancer binding factor 1/T cell-specific factor mediates cooperative signaling by the transforming growth factor-beta and wnt pathways.
    Proc Natl Acad Sci U S A. 2000 Jul 18;97(15):8358-63 PMID: 10890911
  75. Wnt signaling and cancer.
    Genes Dev. 2000 Aug 1;14(15):1837-51 PMID: 10921899
  76. Patterning the early zebrafish by the opposing actions of bozozok and vox/vent.
    Dev Biol. 2000 Aug 15;224(2):275-85 PMID: 10926766
  77. 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
  78. 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
  79. An old enigma: the gray crescent of amphibian eggs.
    Curr Top Dev Biol. 1977;11:133-86 PMID: 332453
  80. High-frequency twinning of Xenopus laevis embryos from eggs centrifuged before first cleavage.
    Dev Biol. 1986 Jul;116(1):228-40 PMID: 3488238
  81. 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
  82. The entire mesodermal mantle behaves as Spemann's organizer in dorsoanterior enhanced Xenopus laevis embryos.
    Dev Biol. 1988 May;127(1):64-77 PMID: 3282938
  83. 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 Mar;114(3):583-97 PMID: 1618130
  84. Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos.
    Cell. 1992 Sep 4;70(5):829-40 PMID: 1339313
  85. Nodal is a novel TGF-beta-like gene expressed in the mouse node during gastrulation.
    Nature. 1993 Feb 11;361(6412):543-7 PMID: 8429908
  86. A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse.
    Development. 1994 Jul;120(7):1919-28 PMID: 7924997
  87. Dorsal midline fate in Drosophila embryos requires twisted gastrulation, a gene encoding a secreted protein related to human connective tissue growth factor.
    Genes Dev. 1994 Jul 1;8(13):1489-501 PMID: 7958834
  88. Dorsal-ventral patterning of the Drosophila embryo depends on a putative negative growth factor encoded by the short gastrulation gene.
    Genes Dev. 1994 Nov 1;8(21):2602-16 PMID: 7958919
  89. Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes.
    Cell. 1994 Dec 2;79(5):779-90 PMID: 8001117
  90. Overexpression of cadherins and underexpression of beta-catenin inhibit dorsal mesoderm induction in early Xenopus embryos.
    Cell. 1994 Dec 2;79(5):791-803 PMID: 7528101
  91. A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin.
    Nature. 1995 Jul 20;376(6537):249-53 PMID: 7617035
  92. New gene, nel, encoding a M(r) 93 K protein with EGF-like repeats is strongly expressed in neural tissues of early stage chick embryos.
    Dev Dyn. 1995 Jun;203(2):212-22 PMID: 7655083
  93. Nodal-related signals induce axial mesoderm and dorsalize mesoderm during gastrulation.
    Development. 1995 Nov;121(11):3651-62 PMID: 8582278
  94. Molecular mechanisms of Spemann's organizer formation: conserved growth factor synergy between Xenopus and mouse.
    Genes Dev. 1995 Dec 15;9(24):3038-50 PMID: 8543150
  95. A common plan for dorsoventral patterning in Bilateria.
    Nature. 1996 Mar 7;380(6569):37-40 PMID: 8598900
  96. TGF-beta signals and a pattern in Xenopus laevis endodermal development.
    Development. 1996 Mar;122(3):1007-15 PMID: 8631246
  97. Microtubule-mediated transport of organelles and localization of beta-catenin to the future dorsal side of Xenopus eggs.
    Proc Natl Acad Sci U S A. 1997 Feb 18;94(4):1224-9 PMID: 9037034
  98. Establishment of the dorso-ventral axis in Xenopus embryos is presaged by early asymmetries in beta-catenin that are modulated by the Wnt signaling pathway.
    J Cell Biol. 1997 Mar 10;136(5):1123-36 PMID: 9060476
  99. Dynamic microtubules and specification of the zebrafish embryonic axis.
    Curr Biol. 1997 Jan 1;7(1):31-42 PMID: 9024620
  100. Frzb-1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer.
    Cell. 1997 Mar 21;88(6):747-56 PMID: 9118218
  101. Frzb, a secreted protein expressed in the Spemann organizer, binds and inhibits Wnt-8.
    Cell. 1997 Mar 21;88(6):757-66 PMID: 9118219
  102. Xnr4: a Xenopus nodal-related gene expressed in the Spemann organizer.
    Dev Biol. 1997 Apr 15;184(2):367-72 PMID: 9133442
  103. The dorsalizing and neural inducing gene follistatin is an antagonist of BMP-4.
    Mech Dev. 1997 Apr;63(1):39-50 PMID: 9178255
  104. The zebrafish organizer requires chordino.
    Nature. 1997 Jun 26;387(6636):862-3 PMID: 9202118
  105. The mouse Fused locus encodes Axin, an inhibitor of the Wnt signaling pathway that regulates embryonic axis formation.
    Cell. 1997 Jul 11;90(1):181-92 PMID: 9230313
  106. Combinatorial signaling by Twisted Gastrulation and Decapentaplegic.
    Mech Dev. 1997 Jun;64(1-2):61-75 PMID: 9232597
  107. Head induction by simultaneous repression of Bmp and Wnt signalling in Xenopus.
    Nature. 1997 Oct 2;389(6650):517-9 PMID: 9333244
Article Info
Journal
Nature reviews. Genetics
Abbr.
Nat Rev Genet
ISSN
1471-0056
Published
2000-12-00
Pages
171-81
Language
English
Region
England
NLM ID
100962779
PMCID
PMC2291143
Subset
IM
Grants
NICHD NIH HHS · R37 HD021502 · United States
NICHD NIH HHS · R37 HD021502-14 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]