Home LiteratureArticle Details
PMID: 10662781 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Requirement for beta-catenin in anterior-posterior axis formation in mice.

The Journal of cell biology ·Vol. 148 ·No. 3 ·2000-02-07 ·Pages 567-78

Huelsken J, Vogel R, Brinkmann V, Erdmann B, Birchmeier C, Birchmeier W

Abstract

The anterior-posterior axis of the mouse embryo is defined before formation of the primitive streak, and axis specification and subsequent anterior development involves signaling from both embryonic ectoderm and visceral endoderm. Tauhe Wnt signaling pathway is essential for various developmental processes, but a role in anterior-posterior axis formation in the mouse has not been previously established. Beta-catenin is a central player in the Wnt pathway and in cadherin-mediated cell adhesion. We generated beta-catenin-deficient mouse embryos and observed a defect in anterior-posterior axis formation at embryonic day 5.5, as visualized by the absence of Hex and Hesx1 and the mislocation of cerberus-like and Lim1 expression. Subsequently, no mesoderm and head structures are generated. Intercellular adhesion is maintained since plakoglobin substitutes for beta-catenin. Our data demonstrate that beta-catenin function is essential in anterior-posterior axis formation in the mouse, and experiments with chimeric embryos show that this function is required in the embryonic ectoderm.

MeSH Terms
Animals Body Patterning/physiology Cytoskeletal Proteins/genetics,physiology Ectoderm/physiology,ultrastructure Embryonic and Fetal Development/physiology Mice Phenotype Trans-Activators beta Catenin
Chemicals
CTNNB1 protein, mouse Cytoskeletal Proteins Trans-Activators beta Catenin
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Huelsken J
Max-Delbrueck-Center for Molecular Medicine, 13125 Berlin, Germany.
Vogel R
Brinkmann V
Erdmann B
Birchmeier C
Birchmeier W
References (85)
85 references, click to expand
  1. Anterior endomesoderm specification in Xenopus by Wnt/beta-catenin and TGF-beta signalling pathways.
    Dev Biol. 1999 May 15;209(2):282-97 PMID: 10328921
  2. Single amino acid substitutions in proteins of the armadillo gene family abolish their binding to alpha-catenin.
    J Biol Chem. 1996 Jan 19;271(3):1520-6 PMID: 8576147
  3. The amino-terminal domain of desmoplakin binds to plakoglobin and clusters desmosomal cadherin-plakoglobin complexes.
    J Cell Biol. 1997 Nov 3;139(3):773-84 PMID: 9348293
  4. Patterning the Xenopus blastula.
    Development. 1997 Nov;124(21):4179-91 PMID: 9334267
  5. Wnt signaling: a common theme in animal development.
    Genes Dev. 1997 Dec 15;11(24):3286-305 PMID: 9407023
  6. The tumor suppressor gene Smad4/Dpc4 is required for gastrulation and later for anterior development of the mouse embryo.
    Genes Dev. 1998 Jan 1;12(1):107-19 PMID: 9420335
  7. 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
  8. Mouse gastrulation: the formation of a mammalian body plan.
    Mech Dev. 1997 Nov;68(1-2):3-25 PMID: 9431800
  9. Cerberus-like is a secreted factor with neutralizing activity expressed in the anterior primitive endoderm of the mouse gastrula.
    Mech Dev. 1997 Nov;68(1-2):45-57 PMID: 9431803
  10. Formation and function of Spemann's organizer.
    Annu Rev Cell Dev Biol. 1997;13:611-67 PMID: 9442883
  11. Hex: a homeobox gene revealing peri-implantation asymmetry in the mouse embryo and an early transient marker of endothelial cell precursors.
    Development. 1998 Jan;125(1):85-94 PMID: 9389666
  12. Sequential roles for Otx2 in visceral endoderm and neuroectoderm for forebrain and midbrain induction and specification.
    Development. 1998 Mar;125(5):845-56 PMID: 9449667
  13. Regulation of the Hedgehog and Wingless signalling pathways by the F-box/WD40-repeat protein Slimb.
    Nature. 1998 Jan 29;391(6666):493-6 PMID: 9461217
  14. Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3beta and beta-catenin and promotes GSK-3beta-dependent phosphorylation of beta-catenin.
    EMBO J. 1998 Mar 2;17(5):1371-84 PMID: 9482734
  15. The type I activin receptor ActRIB is required for egg cylinder organization and gastrulation in the mouse.
    Genes Dev. 1998 Mar 15;12(6):844-57 PMID: 9512518
  16. Smad2 signaling in extraembryonic tissues determines anterior-posterior polarity of the early mouse embryo.
    Cell. 1998 Mar 20;92(6):797-808 PMID: 9529255
  17. Functional interaction of an axin homolog, conductin, with beta-catenin, APC, and GSK3beta.
    Science. 1998 Apr 24;280(5363):596-9 PMID: 9554852
  18. Expression of the mouse cerberus-related gene, Cerr1, suggests a role in anterior neural induction and somitogenesis.
    Proc Natl Acad Sci U S A. 1998 May 26;95(11):6198-203 PMID: 9600941
  19. Mutations in the homeobox gene HESX1/Hesx1 associated with septo-optic dysplasia in human and mouse.
    Nat Genet. 1998 Jun;19(2):125-33 PMID: 9620767
  20. Failure of egg cylinder elongation and mesoderm induction in mouse embryos lacking the tumor suppressor smad2.
    Proc Natl Acad Sci U S A. 1998 Aug 4;95(16):9378-83 PMID: 9689088
  21. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4.
    Nat Genet. 1998 Aug;19(4):379-83 PMID: 9697701
  22. The C-terminal transactivation domain of beta-catenin is necessary and sufficient for signaling by the LEF-1/beta-catenin complex in Xenopus laevis.
    Mech Dev. 1999 Mar;81(1-2):65-74 PMID: 10330485
  23. Nuclear beta-catenin and the development of bilateral symmetry in normal and LiCl-exposed chick embryos.
    Development. 1999 Jul;126(13):2955-65 PMID: 10357939
  24. Requirement for Wnt3 in vertebrate axis formation.
    Nat Genet. 1999 Aug;22(4):361-5 PMID: 10431240
  25. Direct regulation of the Xenopus engrailed-2 promoter by the Wnt signaling pathway, and a molecular screen for Wnt-responsive genes, confirm a role for Wnt signaling during neural patterning in Xenopus.
    Mech Dev. 1999 Sep;87(1-2):21-32 PMID: 10495268
  26. Cancer, catenins, and cuticle pattern: a complex connection.
    Science. 1993 Dec 10;262(5140):1667-8 PMID: 8259511
  27. Dynamics of cadherin/catenin complex formation: novel protein interactions and pathways of complex assembly.
    J Cell Biol. 1994 Jun;125(6):1327-40 PMID: 8207061
  28. E-cadherin null mutant embryos fail to form a trophectoderm epithelium.
    Proc Natl Acad Sci U S A. 1994 Aug 16;91(17):8263-7 PMID: 8058792
  29. Identification of the plakoglobin-binding domain in desmoglein and its role in plaque assembly and intermediate filament anchorage.
    J Cell Biol. 1994 Oct;127(1):151-60 PMID: 7929560
  30. Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1-deficient mice.
    Genes Dev. 1994 Nov 15;8(22):2691-703 PMID: 7958926
  31. Distinct cadherin-catenin complexes in Ca(2+)-dependent cell-cell adhesion.
    FEBS Lett. 1994 Nov 28;355(2):195-200 PMID: 7982500
  32. 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
  33. E-cadherin and APC compete for the interaction with beta-catenin and the cytoskeleton.
    J Cell Biol. 1994 Dec;127(6 Pt 2):2061-9 PMID: 7806582
  34. Tumor-suppressor gene products in cell contacts: the cadherin-APC-armadillo connection.
    Curr Opin Cell Biol. 1994 Oct;6(5):711-6 PMID: 7833051
  35. A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development.
    Proc Natl Acad Sci U S A. 1995 Jan 31;92(3):855-9 PMID: 7846066
  36. An HMG-box-containing T-cell factor required for thymocyte differentiation.
    Nature. 1995 Mar 2;374(6517):70-4 PMID: 7870176
  37. Embryonic axis induction by the armadillo repeat domain of beta-catenin: evidence for intracellular signaling.
    J Cell Biol. 1995 Mar;128(5):959-68 PMID: 7876319
  38. Requirement for Lim1 in head-organizer function.
    Nature. 1995 Mar 30;374(6521):425-30 PMID: 7700351
  39. Visceral endoderm-1 (VE-1): an antigen marker that distinguishes anterior from posterior embryonic visceral endoderm in the early post-implantation mouse embryo.
    Mech Dev. 1995 Jan;49(1-2):117-21 PMID: 7538319
  40. Identification of plakoglobin domains required for association with N-cadherin and alpha-catenin.
    J Biol Chem. 1995 Aug 25;270(34):20201-6 PMID: 7650039
  41. Lack of beta-catenin affects mouse development at gastrulation.
    Development. 1995 Nov;121(11):3529-37 PMID: 8582267
  42. Rpx: a novel anterior-restricted homeobox gene progressively activated in the prechordal plate, anterior neural plate and Rathke's pouch of the mouse embryo.
    Development. 1996 Jan;122(1):41-52 PMID: 8565852
  43. Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly.
    Science. 1996 May 17;272(5264):1023-6 PMID: 8638126
  44. The axis-inducing activity, stability, and subcellular distribution of beta-catenin is regulated in Xenopus embryos by glycogen synthase kinase 3.
    Genes Dev. 1996 Jun 15;10(12):1443-54 PMID: 8666229
  45. Functional interaction of beta-catenin with the transcription factor LEF-1.
    Nature. 1996 Aug 15;382(6592):638-42 PMID: 8757136
  46. XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos.
    Cell. 1996 Aug 9;86(3):391-9 PMID: 8756721
  47. Beta-catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos.
    Mech Dev. 1996 Jul;57(2):191-8 PMID: 8843396
  48. Targeted mutation of plakoglobin in mice reveals essential functions of desmosomes in the embryonic heart.
    J Cell Biol. 1996 Oct;135(1):215-25 PMID: 8858175
  49. A new mouse member of the Wnt gene family, mWnt-8, is expressed during early embryogenesis and is ectopically induced by retinoic acid.
    Mech Dev. 1996 Aug;58(1-2):141-52 PMID: 8887323
  50. Nuclear localization of beta-catenin by interaction with transcription factor LEF-1.
    Mech Dev. 1996 Sep;59(1):3-10 PMID: 8892228
  51. Maternal beta-catenin establishes a 'dorsal signal' in early Xenopus embryos.
    Development. 1996 Oct;122(10):2987-96 PMID: 8898213
  52. Embryonic heart and skin defects in mice lacking plakoglobin.
    Dev Biol. 1996 Dec 15;180(2):780-5 PMID: 8954745
  53. An alpha-E-catenin gene trap mutation defines its function in preimplantation development.
    Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):901-6 PMID: 9023354
  54. nodal expression in the primitive endoderm is required for specification of the anterior axis during mouse gastrulation.
    Development. 1997 Mar;124(5):1033-44 PMID: 9056778
  55. 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
  56. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC.
    Science. 1997 Mar 21;275(5307):1787-90 PMID: 9065402
  57. Stabilization of beta-catenin by genetic defects in melanoma cell lines.
    Science. 1997 Mar 21;275(5307):1790-2 PMID: 9065403
  58. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF.
    Cell. 1997 Mar 21;88(6):789-99 PMID: 9118222
  59. The roles of maternal alpha-catenin and plakoglobin in the early Xenopus embryo.
    Development. 1997 Apr;124(8):1553-60 PMID: 9108371
  60. Characterization of the interactions of alpha-catenin with alpha-actinin and beta-catenin/plakoglobin.
    J Cell Sci. 1997 Apr;110 ( Pt 8):1013-22 PMID: 9152027
  61. A role for Siamois in Spemann organizer formation.
    Development. 1997 Jul;124(13):2581-9 PMID: 9217000
  62. Armadillo and dTCF: a marriage made in the nucleus.
    Curr Opin Genet Dev. 1997 Aug;7(4):459-66 PMID: 9309175
  63. Analysis of the signaling activities of localization mutants of beta-catenin during axis specification in Xenopus.
    J Cell Biol. 1997 Oct 6;139(1):229-43 PMID: 9314542
  64. 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
  65. Identification of c-MYC as a target of the APC pathway.
    Science. 1998 Sep 4;281(5382):1509-12 PMID: 9727977
  66. An assessment of the developmental potential of embryonic stem cells in the midgestation mouse embryo.
    Development. 1989 Apr;105(4):733-7 PMID: 2598811
  67. Expression of multiple novel Wnt-1/int-1-related genes during fetal and adult mouse development.
    Genes Dev. 1990 Dec;4(12B):2319-32 PMID: 2279700
  68. A homolog of the armadillo protein in Drosophila (plakoglobin) associated with E-cadherin.
    Science. 1991 Nov 29;254(5036):1359-61 PMID: 1962194
  69. The Wnt family of cell signalling molecules in postimplantation development of the mouse.
    Ciba Found Symp. 1992;165:199-212; discussion 212-8 PMID: 1516469
  70. 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
  71. beta-catenin is a target for the ubiquitin-proteasome pathway.
    EMBO J. 1997 Jul 1;16(13):3797-804 PMID: 9233789
  72. Misexpression of Cwnt8C in the mouse induces an ectopic embryonic axis and causes a truncation of the anterior neuroectoderm.
    Development. 1997 Aug;124(15):2997-3005 PMID: 9247341
  73. A beta-catenin/XTcf-3 complex binds to the siamois promoter to regulate dorsal axis specification in Xenopus.
    Genes Dev. 1997 Sep 15;11(18):2359-70 PMID: 9308964
  74. Evidence for a frizzled-mediated wnt pathway required for zebrafish dorsal mesoderm formation.
    Development. 1998 Nov;125(21):4283-92 PMID: 9753682
  75. Pattern formation in zebrafish--fruitful liaisons between embryology and genetics.
    Curr Top Dev Biol. 1999;41:1-35 PMID: 9784971
  76. Function of zebrafish beta-catenin and TCF-3 in dorsoventral patterning.
    Mech Dev. 1998 Sep;77(1):63-74 PMID: 9784608
  77. Cripto is required for correct orientation of the anterior-posterior axis in the mouse embryo.
    Nature. 1998 Oct 15;395(6703):702-7 PMID: 9790191
  78. Visceral endoderm-restricted translation of Otx1 mediates recovery of Otx2 requirements for specification of anterior neural plate and normal gastrulation.
    Development. 1998 Dec;125(24):5091-104 PMID: 9811592
  79. Differential molecular interactions of beta-catenin and plakoglobin in adhesion, signaling and cancer.
    Curr Opin Cell Biol. 1998 Oct;10(5):629-39 PMID: 9818174
  80. De Novo hair follicle morphogenesis and hair tumors in mice expressing a truncated beta-catenin in skin.
    Cell. 1998 Nov 25;95(5):605-14 PMID: 9845363
  81. Conservation of intracellular Wnt signaling components in dorsal-ventral axis formation in zebrafish.
    Dev Genes Evol. 1999 Jan;209(1):48-58 PMID: 9914418
  82. Axis development and early asymmetry in mammals.
    Cell. 1999 Jan 22;96(2):195-209 PMID: 9988215
  83. The oncogenic activation of beta-catenin.
    Curr Opin Genet Dev. 1999 Feb;9(1):15-21 PMID: 10072352
  84. The EGF-CFC protein one-eyed pinhead is essential for nodal signaling.
    Cell. 1999 Apr 2;97(1):121-32 PMID: 10199408
  85. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells.
    Nature. 1999 Apr 1;398(6726):422-6 PMID: 10201372
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
DOI
10.1083/jcb.148.3.567
Published
2000-02-07
Pages
567-78
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2174807
Subset
IM
External Links
PubMed source DOI: 10.1083/jcb.148.3.567 PMC Full Text View journal details
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]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2