Skip to main content

Wnt Signaling Networks and Embryonic Patterning

  • Chapter
Rise and Fall of Epithelial Phenotype

Part of the book series: Molecular Biology Intelligence Unit ((MBIU))

  • 704 Accesses

Abstract

Wnt signaling lies at the heart of metazoan development. The Wnt pathway bifurcates a number of times and regulates cell polarity, migration, adhesion and gene expression. I review the complexity of this network with a focus on the role of SOX proteins in its regulation.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Muller WE, Bohm M, Grebenjuk VA et al. Conservation of the positions of metazoan introns from sponges to humans. Gene 2002; 295(2):299–309.

    PubMed  Google Scholar 

  2. Pires-daSilva A, Sommer RJ. The evolution of signalling pathways in animal development. Nat Rev Genet 2003; 4(1):39–49.

    PubMed  CAS  Google Scholar 

  3. Willert K, Brown JD, Danenberg E et al. Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 2003; 423(6938):448–52.

    PubMed  CAS  Google Scholar 

  4. Hobmayer E, Hatta M, Fischer R et al. Identification of a Hydra homologue of the beta-catenin/plakoglobin/armadillo gene family. Gene 1996; 172(1):155–9.

    PubMed  CAS  Google Scholar 

  5. Hobmayer B, Rentzsch F, Kuhn K et al. WNT signalling molecules act in axis formation in the diploblastic metazoan Hydra. Nature 2000; 407(6801):186–9.

    PubMed  CAS  Google Scholar 

  6. Steele RE. Developmental signaling in Hydra: What does it take to build a “simple” animal? Dev Biol 2002; 248(2):199–219.

    PubMed  CAS  Google Scholar 

  7. King N, Carroll SB. A receptor tyrosine kinase from choanoflagellates: Molecular insights into early animal evolution. Proc Natl Acad Sci USA 2001; 98(26):15032–7.

    PubMed  CAS  Google Scholar 

  8. Snell EA, Furlong RF, Holland PW. Hsp70 sequences indicate that choanoflagellates are closely related to animals. Curr Biol 2001; 11(12):967–70.

    PubMed  CAS  Google Scholar 

  9. Lang BF, O’Kelly C, Nerad T et al. The closest unicellular relatives of animals. Curr Biol 2002; 12(20):1773–8.

    PubMed  CAS  Google Scholar 

  10. Rokas A, King N, Finnerty J et al. Conflicting phylogenetic signals at the base of the metazoan tree. Evol Dev 2003; 5(4):346–59.

    PubMed  CAS  Google Scholar 

  11. King N, Hittinger CT, Carroll SB. Evolution of key cell signaling and adhesion protein families predated the origin of animals. Science 2003; 301:361–163.

    PubMed  CAS  Google Scholar 

  12. Grimson MJ, Coates JC, Reynolds JP et al. Adherens junctions and beta-catenin-mediated cell signalling in a nonmetazoan organism. Nature 2000; 408(6813):727–31.

    PubMed  CAS  Google Scholar 

  13. Hendriks B, Reichmann E. Wnt signaling: A complex issue. Biol Res 2002; 35(2):277–86.

    Article  PubMed  CAS  Google Scholar 

  14. Pandur P, Maurus D, Kuhl M. Increasingly complex: New players enter the Wnt signaling net work. Bioessays 2002; 24(10):881–4.

    PubMed  CAS  Google Scholar 

  15. Reya T, Duncan AW, Allies L et al. A role for Wnt signalling in self-renewal of haematopoietic stem cells. Nature 2003; 423(6938):409–14.

    PubMed  CAS  Google Scholar 

  16. Wu J, Saint-Jeannet JP, Klein PS. Wnt-frizzled signaling in neural crest formation. Trends Neurosci 2003; 26(1):40–5.

    PubMed  CAS  Google Scholar 

  17. Miller JR. The Wnts. Genome Biol 2002; 3(1):REVIEWS3001.

    Google Scholar 

  18. Behrens J. Cross-regulation of the Wnt signalling pathway: A role of MAP kinases. J Cell Sci 2000; 113 (Pt 6):911–9.

    PubMed  CAS  Google Scholar 

  19. Korswagen HC. Canonical and noncanonical Wnt signaling pathways in Caenorhabditis elegans: Variations on a common signaling theme. Bioessays 2002; 24(9):801–10.

    PubMed  CAS  Google Scholar 

  20. Malbon CC, Wang H, Moon RT. Wnt signaling and heterotrimeric G-proteins: Strange bedfel lows or a classic romance? Biochem Biophys Res Commun 2001; 287(3):589–93.

    PubMed  CAS  Google Scholar 

  21. Tamai K, Semenov M, Kato Y et al. LDL-receptor-related proteins in Wnt signal transduction. Nature 2000; 407(6803):530–5.

    PubMed  CAS  Google Scholar 

  22. Wehrli M, Dougan ST, Caldwell K et al. arrow encodes an LDL-receptor-related protein essential for wingless signalling. Nature 2000; 407(6803):527–30.

    PubMed  CAS  Google Scholar 

  23. Fujino T, Asaba H, Kang MJ. et al. Low-density lipoprotein receptor-related protein 5 (LRP5) is essential for normal cholesterol metabolism and glucose-induced insulin secretion. Proc Natl Acad Sci USA 2003; 100(1):229–34.

    PubMed  CAS  Google Scholar 

  24. Mao J, Wang J, Liu B et al. Low-density lipoprotein receptor-related protein-5 binds to Axin and regulates the canonical Wnt signaling pathway. Mol Cell 2001; 7(4):801–9.

    PubMed  CAS  Google Scholar 

  25. Wu W, Glinka A, Delius H et al. Mutual antagonism between dickkopf1 and dickkopf2 regulates Wnt/beta-catenin signalling. Curr Biol 2000; 10(24):1611–4.

    PubMed  CAS  Google Scholar 

  26. Itasaki N, Jones CM, Mercurio S et al. Wise, a context-dependent activator and inhibitor of Wnt signalling. Development 2003; 130(18):4295–305.

    PubMed  CAS  Google Scholar 

  27. Mao B, Wu W, Davidson G et al. Kremen proteins are Dickkopf receptors that regulate Wnt/beta-catenin signalling. Nature 2002; 417(6889):664–7.

    PubMed  CAS  Google Scholar 

  28. Mao B, Niehrs C. Kremen2 modulates Dickkopf2 activity during Wnt/1RP6 signaling. Gene 2003; 302(1–2):179–83.

    PubMed  CAS  Google Scholar 

  29. Jones SE, Jomary C. Secreted Frizzled-related proteins: Searching for relationships and patterns. Bioessays 2002; 24(9):811–20.

    PubMed  CAS  Google Scholar 

  30. Yoshikawa S, McKinnon RD, Kokel M et al. Wnt-mediated axon guidance via the Drosophila Derailed receptor. Nature 2003; 422(6932):583–8.

    PubMed  CAS  Google Scholar 

  31. Halford MM, Stacker SA. Revelations of the RYK receptor. Bioessays 2001; 23(1):34–45.

    PubMed  CAS  Google Scholar 

  32. Yoshikawa S, Bonkowsky JL, Kokel M et al. The derailed guidance receptor does not require kinase activity in vivo. J Neurosci 2001; 21(1):RC119.

    PubMed  CAS  Google Scholar 

  33. Patthy L. The WIF module. Trends Biochem Sci 2000; 25(1):12–3.

    PubMed  CAS  Google Scholar 

  34. Medina A, Reintsch W, Steinbeisser H. Xenopus frizzled 7 can act in canonical and noncanonical Wnt signaling pathways: Implications on early patterning and morphogenesis. Mech Dev 2000; 92(2):227–37.

    PubMed  CAS  Google Scholar 

  35. Boutros M, Paricio N, Strutt DI et al. Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling. Cell 1998; 94(1):109–18.

    PubMed  CAS  Google Scholar 

  36. Boutros M, Mlodzik M. Dishevelled: At the crossroads of divergent intracellular signaling path ways. Mech Dev 1999; 83(1–2):27–37.

    PubMed  CAS  Google Scholar 

  37. Axelrod JD, Matsuno K, Artavanis TS et al. Interaction between Wingless and Notch signaling pathways mediated by dishevelled. Science 1996; 271(5257):1826–32.

    PubMed  CAS  Google Scholar 

  38. Habas R, Dawid IB, He X. Coactivation of Rac and Rho by Wnt/Frizzled signaling is required for vertebrate gastruiation. Genes Dev 2003; 17(2):295–309.

    PubMed  CAS  Google Scholar 

  39. Weston CR, Davis RJ. The JNK signal transduction pathway. Curr Opin Genet Dev 2002; 12(1):14–21.

    PubMed  CAS  Google Scholar 

  40. Zhang Y, Neo SY, Wang X et al. Axin forms a complex with MEKK1 and activates c-Jun NH(2)-terminal kinase/stress-activated protein kinase through domains distinct from Wnt signaling. J Biol Chem 1999; 274(49):35247–54.

    PubMed  CAS  Google Scholar 

  41. Zhang Y, Neo SY, Han J et al. Dimerization choices control the ability of axin and dishevelled to activate c-Jun N-terminal kinase/stress-activated protein kinase. J Biol Chem 2000; 275(32):25008–14.

    PubMed  CAS  Google Scholar 

  42. Cheyette BN, Waxman JS, Miller JR et al. Dapper, a Dishevelled-associated antagonist of beta-catenin and JNK signaling, is required for notochord formation. Dev Cell 200; 2(4):449–61.

    Google Scholar 

  43. Gloy J, Hikasa H, Sokol SY. Frodo interacts with Dishevelled to transduce Wnt signals. Nat Cell Biol 2002; 4(5):351–7.

    PubMed  CAS  Google Scholar 

  44. Katoh M. Identification and characterization of human DAPPER1 and DAPPER2 genes in silico. Int J Oncol 2003; 22(4):907–13.

    PubMed  CAS  Google Scholar 

  45. Thieffry D, Romero D. The modularity of biological regulatory networks. Biosystems 1999; 50(1):49–59.

    PubMed  CAS  Google Scholar 

  46. Jong de, Modeling H. Modeling and simulation of genetic regulatory systems: A literature review. J Comput Biol 2002; 9(1):67–103.

    PubMed  Google Scholar 

  47. Muller HJ. Further studies on the nature and causes of gene mutations. Sixth Int Cong Genet 1932; 1:213–255.

    Google Scholar 

  48. Brennan K, Klein T, Wilder E et al. Wingless modulates the effects of dominant negative notch molecules in the developing wing of Drosophila. Dev Biol 1999; 2l6(1):210–29.

    Google Scholar 

  49. Loose M, Patient R. A genetic regulatory network for Xenopus mesendodermal formation. Devel Biol 2004; 271:467–478.

    CAS  Google Scholar 

  50. McMahon AP, Moon RT. Ectopic expression of the proto-oncogene int-1 in Xenopus embryos leads to duplication of the embryonic axis. Cell 1989; 58:1075–1084.

    PubMed  CAS  Google Scholar 

  51. McCrea PD, Brieher WM, Gumbiner BM. Induction of a secondary body axis in Xenopus by antibodies to β-catenin. J Cell Biol 1993; 123(2):477–84.

    PubMed  CAS  Google Scholar 

  52. Heasman J, Crawford A, Goldstone K et al. Overexpression of cadherins and underexpression of β-catenin inhibit dorsal mesoderm induction in early Xenopus embryos. Cell 1994; 79:791–803.

    PubMed  CAS  Google Scholar 

  53. Funayama N, Fagotto F, McCrea P et al. Embryonic axis induction by the armadillo repeat domain of beta-catenin: Evidence for intracellular signaling. J Cell Biol 1995; 128(5):959–68.

    PubMed  CAS  Google Scholar 

  54. Karnovsky A, Klymkowsky MW. Anterior axis duplication in Xenopus induced by the over-expression of the cadherin-binding protein plakoglobin. Proc Natl Acad Sci USA 1995; 92(10):4522–6.

    PubMed  CAS  Google Scholar 

  55. Carl TF, Dufton C, Hanken J et al. Inhibition of neural crest migration in Xenopus using antisense slug RNA. Dev Biol 1999; 213(1):101–115.

    PubMed  CAS  Google Scholar 

  56. Houston DW, Kofron M, Resnik E et al. Repression of organizer genes in dorsal and ventral Xenopus cells mediated by maternal XTcf3. Development 2002; 129(17):4015–25.

    PubMed  CAS  Google Scholar 

  57. Spokony RF, Aoki Y, Saint-Germain N et al. The transcription factor Sox9 is required for cranial neural crest development in Xenopus. Development 2002; 129(2):421–32.

    PubMed  CAS  Google Scholar 

  58. Grunz H. Developmental biology of amphibians after Hans spemann in germany. Int J Dev Biol 2001; 45 (1 Spec No):39–50.

    PubMed  CAS  Google Scholar 

  59. Holtfreter JF. A new look at Spemann’s organizer. Dev Biol (N Y 1985) 1988; 5:127–50.

    CAS  Google Scholar 

  60. Schneider SQ, Finnerty JR, Martindale MQ. Protein evolution: Structurerunction relationships of the oncogene beta-catenin in the evolution of multicellular animals. J Exp Zool 2003; 295B(1):25–44.

    CAS  Google Scholar 

  61. Coates JC, Grimson MJ, Williams RS et al. Loss of the beta-catenin homologue aardvark causes ectopic stalk formation in Dictyostelium. Mech Dev 2002; 116(1–2):117–27.

    PubMed  CAS  Google Scholar 

  62. Gelderloos J, Witcher L, Cowin P et al. Plakoglobin: The other ARM of vertebrates. In: Cowin P, Klymkowsky MW, editors. Cytoskeletal-membrane interactions and signal transduction. Austin, Texas: Landes Bioscience, 1997:13–30.

    Google Scholar 

  63. Zhurinsky J, Shtutman M, Ben-Ze’ev A. Plakoglobin and beta-catenin: Protein interactions, regulation and biological roles. J Cell Sci 2000; 113(Pt 18):3127–39.

    PubMed  CAS  Google Scholar 

  64. Natarajan L, Witwer NE, Eisenmann DM. The divergent Caenorhabditis elegans beta-catenin proteins BAR-1, WRM-1 and HMP-2 make distinct protein interactions but retain functional redundancy in vivo. Genetics 2001; 159(1):159–72.

    PubMed  CAS  Google Scholar 

  65. Steinberg MS, McNutt PM. Cadherins and their connections: Adhesion junctions have broader functions. Curr Opin Cell Biol 1999; 11(5):554–60.

    PubMed  CAS  Google Scholar 

  66. Pokutta S, Weis WI. The cytoplasmic face of cell contact sites. Curr Opin Struct Biol 2002; 12(2):255–62.

    PubMed  CAS  Google Scholar 

  67. Perez-Martin J, Espinosa M. A genetic system to study the in vivo role of transcriptional regulators in Escherichia coli. Gene 1992; 116(1):75–80.

    PubMed  CAS  Google Scholar 

  68. Kowalczyk AP, Bornslaeger EA, Norvell SM et al. Desmosomes: Intercellular adhesive junctions specialized for attachment of intermediate filaments. Int Rev Cytol 1999; 185(237):237–302.

    PubMed  CAS  Google Scholar 

  69. Garrod DR, Merritt AJ, Nie Z. Desmosomal adhesion: Structural basis, molecular mechanism and regulation (Review). Mol Membr Biol 2002; 19(2):81–94.

    PubMed  CAS  Google Scholar 

  70. Bierkamp C, Schwarz H, Huber O et al. Desmosomal localization of beta-catenin in the skin of plakoglobin null-mutant mice [In Process Citation]. Development 1999; 126(2):371–81.

    PubMed  CAS  Google Scholar 

  71. Bartnik E, Weber K. Intermediate filaments in the giant muscle cells of the nematode Ascaris lumbricoides; abundance and three-dimensional complexity of arrangements. Eur J Cell Biol 1987; 45:291–301.

    Google Scholar 

  72. Bartnik E, Weber K. Widespread occurrence of intermediate filaments in invertebrates: Common principles and diversion. Eur J Cell Bio 1989; 50:17–33.

    Google Scholar 

  73. Johansen KM, Johansen J. Filarin, a novel invertebrate intermediate filament protein present in axons and perikarya of developing and mature leech neurons. J Neurobiol 1995; 27(2):227–39.

    PubMed  CAS  Google Scholar 

  74. Karabinos A, Schmidt H, Harborth J et al. Essential roles for four cytoplasmic intermediate filament proteins in Caenorhabditis elegans development. Proc Natl Acad Sci USA 2001; 98(14):7863–8.

    PubMed  CAS  Google Scholar 

  75. Kofron M, Spagnuolo A, Klymkowsky M et al. The roles of maternal alpha-catenin and plakoglobin in the early Xenopus embryo. Development 1997; 124(8):1553–60.

    PubMed  CAS  Google Scholar 

  76. St Amand AL, Klymkowsky MW. Cadherins and catenins, Wnts and SOXs: Embryonic patterning in Xenopus. Int Rev Cytol 2001; 203:291–355.

    Article  PubMed  CAS  Google Scholar 

  77. Williams BO, Barish GD, Klymkowsky MW et al. A comparative evaluation of beta-catenin and plakoglobin signaling activity. Oncogene 2000; 19(50):5720–8.

    PubMed  CAS  Google Scholar 

  78. Posthaus H, Williamson L, Baumann D et al. Beta-Catenin is not required for proliferation and differentiation of epidermal mouse keratinocytes. J Cell Sci 2002; 115(Pt 23):4587–95.

    PubMed  CAS  Google Scholar 

  79. Fagotto F, Gluck U, Gumbiner BM. Nuclear localization signal-independent and importin/karyopherin-independent nuclear import of beta-catenin. Curr Biol 1998; 8(4):181–90.

    PubMed  CAS  Google Scholar 

  80. Yokoya F, Imamoto N, Tachibana T et al. Beta-catenin can be transported into the nucleus in a Ran-unassisted manner. Mol Biol Cell 1999; 10(4):1119–31.

    PubMed  CAS  Google Scholar 

  81. Lee SJ, Imamoto N, Sakai H et al. The adoption of a twisted structure of importin-beta is essential for the protein-protein interaction required for nuclear transport. J Mol Biol 2000; 302(1):251–64.

    PubMed  CAS  Google Scholar 

  82. Riggleman B, Wieschaus E, Schedl P. Molecular analysis of the armadillo locus: Uniformly distributed transcripts and a protein with novel internal repeats are associated with a Drosophila segment polarity gene. Genes Dev 1989; 3(1):96–113.

    PubMed  CAS  Google Scholar 

  83. White P, Aberle H, Vincent JP. Signaling and adhesion activities of mammalian beta-catenin and plakoglobin in drosophila. J Cell Biol 1998; 140(1):183–95.

    PubMed  CAS  Google Scholar 

  84. Wharton KA, Jr. Runnin’ with the Dvl: Proteins that associate with Dsh/Dvl and their significance to Wnt signal transduction. Dev Biol 2003; 253(1):1–17.

    PubMed  CAS  Google Scholar 

  85. Ahumada A, Slusarski DC, Liu X et al. Signaling of rat Frizzled-2 through phosphodiesterase and cyclic GMP. Science 2002; 298(5600):2006–10.

    PubMed  CAS  Google Scholar 

  86. Ishitani T, Kishida S, Hyodo-Miura J et al. The TAK1-NLK mitogen-activated protein kinase cascade functions in the Wnt-5a/Ca(2+) pathway to antagonize Wnt/beta-catenin signaling. Mol Cell Biol 2003; 23(1):131–9.

    PubMed  CAS  Google Scholar 

  87. Capelluto DG, Kutateladze TG, Habas R et al. The DIX domain targets dishevelled to actin stress fibres and vesicular membranes. Nature 2002; 419(6908):726–9.

    PubMed  CAS  Google Scholar 

  88. Tanaka M, Kamo T, Ota S et al. Association of Dishevelled with Eph tyrosine kinase receptor and ephrin mediates cell repulsion. Embo J 2003; 22(4):847–58.

    PubMed  CAS  Google Scholar 

  89. Aberle H, Bauer A, Stappert J et al. β-catenin is a target for the ubiquitin-proteasome pathway. Embo J 1997; 16(13):3797–804.

    PubMed  CAS  Google Scholar 

  90. Wiechens N, Fagotto F. CRM1-and Ran-independent nuclear export of beta-catenin. Curr Biol 2001; 11(1):18–27.

    PubMed  CAS  Google Scholar 

  91. Leung JY, Kolligs FT, Wu R et al. Activation of AXIN2 expression by beta-catenin-T cell factor. A feedback repressor pathway regulating Wnt signaling. J Biol Chem 2002; 277(24):21657–65.

    PubMed  CAS  Google Scholar 

  92. Hulsken J, Birchmeier W, Behrens J. E-cadherin and APC compete for the interaction with beta-catenin and the cytoskeleton. J Cell Biol 1994:2061–9.

    Google Scholar 

  93. Rubinfeld B, Souza B, Albert I et al. The APC protein and E-cadherin form similar but independent complexes with alpha-catenin, beta-catenin, and plakoglobin. J Biol Chem 1995; 270(10):5549–55.

    PubMed  CAS  Google Scholar 

  94. Klymkowsky MW, Williams BO, Barish GD et al. Membrane-anchored plakoglobins have multiple mechanisms of action in Wnt signaling. Mol Biol Cell 1999; 10(10):3151–3169.

    PubMed  CAS  Google Scholar 

  95. Kodama S, Ikeda S, Asahara T et al. Axin directly interacts with plakoglobin and regulates its stability. J Biol Chem 1999; 274(39):27682–8.

    PubMed  CAS  Google Scholar 

  96. Rubenstein A, Merriam J, Klymkowsky MW. Localizing the adhesive and signaling functions of plakoglobin. Dev Genet 1997; 20(2):91–102.

    PubMed  CAS  Google Scholar 

  97. Simcha I, Geiger B, Yehuda-Levenberg S et al. Suppression of tumorigenicity by plakoglobin: An augmenting effect of N-cadherin. J Cell Biol 1996; 133:199–209.

    PubMed  CAS  Google Scholar 

  98. Kolligs FT, Kolligs B, Hajra KM et al. Gamma-catenin is regulated by the APC tumor suppressor and its oncogenic activity is distinct from that of beta-catenin. Genes Dev 2000; 14(11):1319–31.

    PubMed  CAS  Google Scholar 

  99. Shtutman M, Zhurinsky J, Oren M et al. PML is a target gene of beta-catenin and plakoglobin, and coactivates beta-catenin-mediated transcription. Cancer Res 2002; 62(20):5947–54.

    PubMed  CAS  Google Scholar 

  100. Winn RA, Bremnes RM, Bemis L et al. Gamma-Catenin expression is reduced or absent in a subset of human lung cancers and reexpression inhibits transformed cell growth. Oncogene 2002; 21(49):7497–506.

    PubMed  CAS  Google Scholar 

  101. Rosin-Arbesfeld R, Townsley F, Bienz M. The APC tumour suppressor has a nuclear export function. Nature 2000; 406(6799):1009–12.

    PubMed  CAS  Google Scholar 

  102. Rosin-Arbesfeld R, Cliffe A, Brabletz T et al. Nuclear export of the APC tumour suppressor controls beta-catenin function in transcription. Embo J 2003; 22(5):1101–13.

    PubMed  CAS  Google Scholar 

  103. Neufeld KL, Nix DA, Bogerd H et al. Adenomatous polyposis coli protein contains two nuclear export signals and shuttles between the nucleus and cytoplasm. Proc Natl Acad Sci USA 2000; 97(22):12085–90.

    PubMed  CAS  Google Scholar 

  104. Neufeld KL, White RL. Nuclear and cytoplasmic localizations of the adenomatous polyposis coli protein. Proc Natl Acad Sci USA 1997; 94(7):3034–9.

    PubMed  CAS  Google Scholar 

  105. Fodde R, Kuipers J, Rosenberg C et al. Mutations in the APC tumour suppressor gene cause chromosomal instability. Nat Cell Biol 2001; 3(4):433–8.

    PubMed  CAS  Google Scholar 

  106. McCartney BM, McEwen DG, Grevengoed E et al. Drosophila APC2 and Armadillo participate in tethering mitotic spindles to cortical actin. Nat Cell Biol 2001; 3(10):933–8.

    PubMed  CAS  Google Scholar 

  107. Kaplan KB, Burds AA, Swedlow JR et al. A role for the Adenomatous Polyposis Coli protein in chromosome segregation. Nat Cell Biol 2001; 3(4):429–32.

    PubMed  CAS  Google Scholar 

  108. Townsley FM, Bienz M. Actin-dependent membrane association of a Drosophila epithelial APC protein and its effect on junctional Armadillo. Curr Biol 2000; 10(21):1339–48.

    PubMed  CAS  Google Scholar 

  109. Zumbrunn J, Kinoshita K, Hyman AA et al. Binding of the adenomatous polyposis coli protein to microtubules increases microtubule stability and is regulated by GSK3 beta phosphorylation. Curr Biol 2001; 11(1):44–9.

    PubMed  CAS  Google Scholar 

  110. Jimbo T, Kawasaki Y, Koyama R et al. Identification of a link between the tumour suppressor APC and the kinesin superfamily. Nat Cell Biol 2002; 4(4):323–7.

    PubMed  CAS  Google Scholar 

  111. Cui H, Dong M, Sadhu DN et al. Suppression of kinesin expression disrupts adenomatous polyposis coli (APC) localization and affects beta-catenin turnover in young adult mouse colon (YAMC) epithelial cells. Exp Cell Res 2002; 280(1):12–23.

    PubMed  CAS  Google Scholar 

  112. Kang D, Soriano S, Xia X et al. Presenilin couples the paired phosphorylation of beta-catenin independent of Axin. Implications for beta-Catenin Activation in Tumorigenesis. Cell 2002; 110(6):751.

    PubMed  CAS  Google Scholar 

  113. Kang DE, Soriano S, Frosch MP et al. Presenilin 1 facilitates the constitutive turnover of beta-catenin: Differential activity of Alzheimer’s disease-linked PS 1 mutants in the beta-catenin-signaling pathway. J Neurosci 1999; 19(11):4229–37.

    PubMed  CAS  Google Scholar 

  114. Mak BC, Takemaru K, Kenerson HL et al. The tuberin-hamartin complex negatively regulates Beta-catenin signaling activity. J Biol Chem 2003; 278(8):5947–51.

    PubMed  CAS  Google Scholar 

  115. Marambaud P, Shioi J, Serban G et al. A presenilin-1/gamma-secretase cleavage releases the E-cadherin intracellular domain and regulates disassembly of adherens junctions. Embo J 2002; 21(8):1948–56.

    PubMed  CAS  Google Scholar 

  116. Baki L, Marambaud P, Efthimiopoulos S et al. Presenilin-1 binds cytoplasmic epithelial cadherin, inhibits cadherin/p120 association, and regulates stability and function of the cadherin/catenin adhesion complex. Proc Natl Acad Sci USA 2001; 98(5):2381–6.

    PubMed  CAS  Google Scholar 

  117. Georgakopoulos A, Marambaud P, Efthimiopoulos S et al. Presenilin-1 forms complexes with the cadherin/catenin cell-cell adhesion system and is recruited to intercellular and synaptic contacts. Mol Cell 1999; 4(6):893–902.

    PubMed  CAS  Google Scholar 

  118. Xia X, Qian S, Soriano S et al. Loss of presenilin 1 is associated with enhanced beta-catenin signaling and skin tumorigenesis. Proc Natl Acad Sci USA 2001; 98(19):10863–8.

    PubMed  CAS  Google Scholar 

  119. Price MA, Kalderon D. Proteolysis of the Hedgehog signaling effector Cubitus interruptus requires phosphorylation by Glycogen Synthase Kinase 3 and Casein Kinase 1. Cell 2002; 108(6):823–35.

    PubMed  CAS  Google Scholar 

  120. Jia J, Amanai K, Wang G et al. Shaggy/GSK3 antagonizes Hedgehog signalling by regulating Cubitus interruptus. Nature 2002; 416(6880):548–52.

    PubMed  CAS  Google Scholar 

  121. Foltz DR, Santiago MC, Berechid BE et al. Glycogen synthase kinase-3beta modulates notch signaling and stability. Curr Biol 2002; 12(12):1006–11.

    PubMed  CAS  Google Scholar 

  122. Cohen P, Frame S. The renaissance of GSK3. Nat Rev Mol Cell Biol 2001; 2(10):769–76.

    PubMed  CAS  Google Scholar 

  123. Thomas GM, Frame S, Goedert M et al. A GSK3-binding peptide from FRAT1 selectively inhib its the GSK3-catalysed phosphorylation of axin and beta-catenin. FEBS Lett 1999; 458(2):247–51.

    PubMed  CAS  Google Scholar 

  124. Franca-Koh J, Yeo M, Fraser E et al. Dale TC. The regulation of glycogen synthase kinase-3 nuclear export by Frat/GBP. J Biol Chem 2002; 277(46):43844–8.

    PubMed  CAS  Google Scholar 

  125. Beals CR, Sheridan CM, Turck CW et al. Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science 1997; 275(5308):1930–4.

    PubMed  CAS  Google Scholar 

  126. Huber AH, Weis WI. The structure of the beta-catenin/E-cadherin complex and the molecular basis of diverse ligand recognition by beta-catenin. Cell 2001; 105(3):391–402.

    PubMed  CAS  Google Scholar 

  127. Eklof Spink K, Fridman SG, Weis WI. Molecular mechanisms of beta-catenin recognition by adenomatous polyposis coli revealed by the structure of an APC-beta-catenin complex. Embo J 2001; 20(22):6203–12.

    PubMed  CAS  Google Scholar 

  128. Graham TA, Weaver C, Mao F et al. Crystal structure of a beta-catenin/Tcf complex. Cell 2000; 103(6):885–96.

    PubMed  CAS  Google Scholar 

  129. Poy F, Lepourcelet M, Shivdasani RA et al. Structure of a human Tcf4-beta-catenin complex. Nat Struct Biol 2001; 8(12):1053–7.

    PubMed  CAS  Google Scholar 

  130. Tago K, Nakamura T, Nishita M et al. Inhibition of Wnt signaling by ICAT, a novel beta-catenin-interacting protein. Genes Dev 2000; 14(14):1741–9.

    PubMed  CAS  Google Scholar 

  131. Graham TA, Clements WK, Kimelman D et al. The crystal structure of the beta-catenin/ICAT complex reveals the inhibitory mechanism of ICAT. Mol Cell 2002; 10(3):563–71.

    PubMed  CAS  Google Scholar 

  132. Daniels DL, Weis WI. ICAT inhibits beta-catenin binding to Tcf/Lef-family transcription factors and the general coactivator p300 using independent structural modules. Mol Cell 2002; 10(3):573–84.

    PubMed  CAS  Google Scholar 

  133. Kobayashi M, Kishida S, Fukui A et al. Nuclear localization of Duplin, a beta-catenin-binding protein, is essential for its inhibitory activity on the Wnt signaling pathway. J Biol Chem 2002; 277(8):5816–22.

    PubMed  CAS  Google Scholar 

  134. Song LN, Herrell R, Byers S et al. Beta-catenin binds to the activation function 2 region of the androgen receptor and modulates the effects of the N-terminal domain and TIF2 on ligand-dependent transcription. Mol Cell Biol 2003; 23(5): 1674–87.

    PubMed  CAS  Google Scholar 

  135. Sekiya T, Nakamura T, Kazuki Y et al. Overexpression of Icat induces G(2) arrest and cell death in tumor cell mutants for adenomatous polyposis coli, beta-catenin, or Axin. Cancer Res 2002; 62(11):3322–6.

    PubMed  CAS  Google Scholar 

  136. Waterman ML, Fischer WH, Jones KA. A thymus-specific member of the HMG protein family regulates the human T cell receptor C alpha enhancer. Genes Dev 1991; 5(4):656–69.

    PubMed  CAS  Google Scholar 

  137. Oosterwegel MA, van de Wetering ML, Holstege FC et al. TCF-1, a T cell-specific transcription factor of the HMG box family, interacts with sequence motifs in the TCR beta and TCR delta enhancers. Int Immunol 1991; 3(11): 1189–92.

    PubMed  CAS  Google Scholar 

  138. Travis A, Amsterdam A, Belanger C et al. LEF-1, a gene encoding a lymphoid-specific protein with an HMG domain, regulates T-cell receptor alpha enhancer function. Genes Dev 1991; 5(5):880–94.

    PubMed  CAS  Google Scholar 

  139. Giese K, Cox J, Grosschedl R. The HMG domain of lymphoid enhancer factor 1 bends DNA and facilitates assembly of functional nucleoprotein structures. Cell 1992; 69(1): 185–95.

    PubMed  CAS  Google Scholar 

  140. Bewley CA, Gronenborn AM, Clore GM. Minor groove-binding architectural proteins: Structure, function, and DNA recognition. Annu Rev Biophys Biomol Struct 1998; 27(105):105–31.

    PubMed  CAS  Google Scholar 

  141. Love JJ, Li X, Case DA et al. Structural basis for DNA bending by the architectural transcription factor LEF-1. Nature 1995; 376:791–5.

    PubMed  CAS  Google Scholar 

  142. van Beest M, Dooijes D, van De Wetering M et al. Sequence-specific high mobility group box factors recognize 10-12-base pair minor groove motifs. J Biol Chem 2000; 275(35):27266–73.

    PubMed  Google Scholar 

  143. Behrens J, von Kries JP, Kuhl M et al. Functional interaction of β-catenin with the transcription factor LEF-1. Nature 1996; 382:638–642.

    PubMed  CAS  Google Scholar 

  144. Molenaar M, van de Wetering M, Oosterwegel M et al. XTcf-3 transcription factor mediates β-catenin-induced axis formation in Xenopus embryos. Cell 1996; 86:391–399.

    PubMed  CAS  Google Scholar 

  145. Huber O, Korn R, McLaughlin J et al. Nuclear localization of beta-catenin by interaction with transcription factor LEF-1. Mech Dev 1996; 59(1):3–10.

    PubMed  CAS  Google Scholar 

  146. Klymkowsky MW. Minireviews, minidogmas and mythinformation. BioEssays 1997; 20:537–539.

    Google Scholar 

  147. Roose J, Huls G, van Beest M et al. Synergy between tumor suppressor APC and the beta-catenin-tcf4 target tcfl. Science 1999; 285(5435):1923–6.

    PubMed  CAS  Google Scholar 

  148. Brantjes H, Roose J, van De Wetering M et al. All Tcf HMG box transcription factors interact with Groucho-related corepressors. Nucleic Acids Res 2001; 29(7): 1410–9.

    PubMed  CAS  Google Scholar 

  149. Bruhn L, Munnerlyn A, Grosschedl R. ALY, a context-dependent coactivator of LEF-1 and AML-1, is required for TCRalpha enhancer function. Genes Dev 1997; 11(5):640–53.

    PubMed  CAS  Google Scholar 

  150. Boras K, Hamel PA. Alx4 binding to LEF-1 regulates N-CAM promoter activity. J Biol Chem 2002; 277(2): 1120–7.

    PubMed  CAS  Google Scholar 

  151. Nishita M, Hashimoto MK, Ogata S et al. Interaction between Wnt and TGF-beta signalling pathways during formation of Spemann’s organizer. Nature 2000; 403(6771):781–5.

    PubMed  CAS  Google Scholar 

  152. Labbe E, Letamendia A, Attisano L. 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 USA 2000; 97(15):8358–63.

    PubMed  CAS  Google Scholar 

  153. Ross DA, Kadesch T. The notch intracellular domain can function as a coactivator for LEF-1. Mol Cell Biol 2001; 21(22):7537–44.

    PubMed  CAS  Google Scholar 

  154. Rocheleau CE, Downs WD, Lin R et al. Wnt signaling and an APC-related gene specify endoderm in early C. elegans embryos. Cell 1997; 90(4):707–16.

    PubMed  CAS  Google Scholar 

  155. Thorpe CJ, Schlesinger A, Carter JC et al. Wnt signaling polarizes an early C. elegans blastomere to distinguish endoderm from mesoderm [In Process Citation]. Cell 1997; 90(4):695–705.

    PubMed  CAS  Google Scholar 

  156. Merriam JM, Rubenstein AB, Klymkowsky MW. Cytoplasmically anchored plakoglobin induces a WNT-like phenotype in Xenopus. Dev Biol 1997; 185(1):67–81.

    PubMed  CAS  Google Scholar 

  157. Zecca M, Basler K, Struhl G. Direct and long-range action of a wingless morphogen gradient. Cell 1996; 87(5):833–44.

    PubMed  CAS  Google Scholar 

  158. Tutter AV, Fryer CJ, Jones KA. Chromatin-specific regulation of LEF-1-beta-catenin transcription activation and inhibition in vitro. Genes Dev 2001; 15(24):3342–54.

    PubMed  CAS  Google Scholar 

  159. Snider L, Thirlwell H, Miller JR et al. Inhibition of Tcf3 binding by I-mfa domain proteins. Mol Cell Biol 2001; 21(5): 1866–73.

    PubMed  CAS  Google Scholar 

  160. Kusano S, Raab-Traub N. I-mfa domain proteins interact with Axin and affect its regulation of the Wnt and c-Jun N-terminal kinase signaling pathways. Mol Cell Biol 2002; 22(18):6393–405.

    PubMed  CAS  Google Scholar 

  161. Chan AP, Etkin LD. Patterning and lineage specification in the amphibian embryo. Curr Top Dev Biol 2001; 51:1–67.

    Article  PubMed  CAS  Google Scholar 

  162. Larabell CA, Torres M, Rowning BA et al. 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; 136(5):1123–36.

    PubMed  CAS  Google Scholar 

  163. Schneider S, Steinbeisser H, Warga RM et al. b-catenin translocation into nuclei demarcates the dorsalizing centers in frog and fish embryos. Mech Devel 1996; 57:191–198.

    CAS  Google Scholar 

  164. Roel G, Hamilton FS, Gent Y et al. Lef-1 and Tcf-3 transcription factors mediate tissue-specific Wnt signaling during Xenopus development. Curr Biol 2002; 12(22): 1941–5.

    PubMed  CAS  Google Scholar 

  165. Zorn AM, Barish GD, Williams BO et al. Regulation of Wnt signaling by Sox proteins: XSoxl7 alpha/beta and XSox3 physically interact with beta-catenin. Mol Cell 1999; 4(4):487–98.

    PubMed  CAS  Google Scholar 

  166. Kim CH, Oda T, Itoh M et al. Repressor activity of Headless/Tcf3 is essential for vertebrate head formation. Nature 2000; 407(6806):913–6.

    PubMed  CAS  Google Scholar 

  167. Lemaire P, Garrett N, Gurdon JB. Expression cloning of Siamois, a Xenopus homeobox gene expressed in dorsal-vegetal cells of blastulae and able to induce a complete secondary axis. Cell 1995; 81(1):85–94.

    PubMed  CAS  Google Scholar 

  168. Brannon M, Gomperts M, Sumoy L et al. A b-catenin/XTcf-3 complex binds to the siamois promoter to regulate dorsal axis specificiation in Xenopus. Genes & Devel 1997; 11:2359–2370.

    CAS  Google Scholar 

  169. Roel G, van den Broek O, Spieker N et al. Tcf-1 expression during Xenopus development. Gene Expr Patterns 2003; 3(2): 123–6.

    PubMed  CAS  Google Scholar 

  170. Bowles J, Schepers G, Koopman P. Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev Biol 2000; 227(2):239–55.

    PubMed  CAS  Google Scholar 

  171. Dailey L, Basilico C. Coevolution of HMG domains and homeodomains and the generation of transcriptional regulation by Sox/POU complexes. J Cell Physiol 2001; 186(3):315–28.

    PubMed  CAS  Google Scholar 

  172. Laudet V, Stehelin D, Clevers H. Ancestry and diversity of the HMG box superfamily. Nucleic Acids Res 1993; 21(10):2493–501.

    PubMed  CAS  Google Scholar 

  173. Mertin S, McDowall SG, Harley VR. The DNA-binding specificity of SOX9 and other SOX proteins. Nucleic Acids Res 1999; 27(5): 1359–64.

    PubMed  CAS  Google Scholar 

  174. Zhang C, Basta T, Jensen ED et al. The catenin/VegT-regulated early zygotic gene Xnr5 is a direct target of SOX3 regulation in Xenopus. Development 2003; 130:5609–5624.

    PubMed  CAS  Google Scholar 

  175. Kamachi Y, Uchikawa M, Kondoh H. Pairing SOX off: With partners in the regulation of embryonic development. Trends Genet 2000; 16(4):182–7.

    PubMed  CAS  Google Scholar 

  176. Weiss MA. Floppy SOX: Mutual induced fit in HMG (High-Mobility Group) Box-DNA recognition. Mol Endocrinol 2001; 15(3):353–362.

    PubMed  CAS  Google Scholar 

  177. Schepers GE, Teasdale RD, Koopman P. Twenty pairs of sox: Extent, homology, and nomenclature of the mouse and human sox transcription factor gene families. Dev Cell 2002; 3(2): 167–70.

    PubMed  CAS  Google Scholar 

  178. Uchikawa M, Kamachi Y, Kondoh H. Two distinct subgroups of Group B Sox genes for transcriptional activators and repressors: Their expression during embryonic organogenesis of the chicken. Mech Dev 1999; 84(1–2): 103–20.

    PubMed  CAS  Google Scholar 

  179. Penzel R, Oschwald R, Chen Y et al. Characterization and early embryonic expression of a neural specific transcription factor xSOX3 in Xenopus laevis. Int J Dev Biol 1997; 41(5):667–77.

    PubMed  CAS  Google Scholar 

  180. Avilion AA, Nicolis SK, Pevny LH et al. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 2003; 17(1): 126–40.

    PubMed  CAS  Google Scholar 

  181. Harley VR, Lovell BR, Goodfellow PN et al. The HMG box of SRY is a calmodulin binding domain. Febs Lett 1996; 391(1–2):24–8.

    PubMed  CAS  Google Scholar 

  182. Kamachi Y, Cheah K, Kondoh H. Mechanism of regulatory target selection by the SOX High-Mobility-Group domain proteins as revealed by comparison of SOX1/2/3 and SOX9. Mol Cell Biol 1999; 19(1):107–120.

    PubMed  CAS  Google Scholar 

  183. Hyodo-Miura J, Urushiyama S, Nagai S et al. Involvement of NLK and Sox11 in neural induction in Xenopus development. Genes Cells 2002; 7(5):487–96.

    PubMed  CAS  Google Scholar 

  184. Takash W, Canizares J, Bonneaud N et al. SOX7 transcription factor: Sequence, chromosomal localisation, expression, transactivation and interference with Wnt signalling. Nucleic Acids Res 2001; 29(21):4274–83.

    PubMed  CAS  Google Scholar 

  185. Fawcett SR, Klymkowsky MW. Embryonic expression of Xenopus laevis SOX7. Gene Expression Report 2004; 4:29–33.

    CAS  Google Scholar 

  186. Shiozawa M, Hiraoka Y, Komatsu N et al. Cloning and characterization of Xenopus laevis xSox7 cDNA. Biochim Biophys Acta 1996; 1309(1–2):73–6.

    PubMed  Google Scholar 

  187. Hiraoka Y, Komatsu N, Sakai Y et al. XLS13A and XLS13B: SRY-related genes of Xenopus laevis. Gene 1997; 197(1–2):65–71.

    PubMed  CAS  Google Scholar 

  188. Kishi M, Mizuseki K, Sasai N et al. Requirement of Sox2-mediated signaling for differentiation of early Xenopus neuroectoderm. Development 2000; 127(4):791–800.

    PubMed  CAS  Google Scholar 

  189. Mizuseki K, Kishi M, Shiota K et al. SoxD: An essential mediator of induction of anterior neural tissues in Xenopus embryos. Neuron 1998; 21(1):77–85.

    PubMed  CAS  Google Scholar 

  190. Martin BL, Harland RM. Hypaxial muscle migration during primary myogenesis in Xenopus laevis. Dev Biol 2001; 239(2):270–80.

    PubMed  CAS  Google Scholar 

  191. Honore SM, Aybar MJ, Mayor R. Sox10 is required for the early development of the prospective neural crest in Xenopus embryos. Dev Biol 2003; 260(1):79–96.

    PubMed  CAS  Google Scholar 

  192. Aoki Y, Saint-Germain N, Gyda M et al. Sox10 regulates the development of neural crest-derived melanocytes in Xenopus. Dev Biol 2003; 259(1):19–33.

    PubMed  CAS  Google Scholar 

  193. LaBonne C. Vertebrate development: Wnt signals at the crest. Curr Biol 2002; 12(21):R743–4.

    PubMed  CAS  Google Scholar 

  194. Garcia-Castro MI, Marcelle C, Bronner-Fraser M. Ectodermal Wnt function as a neural crest inducer. Science 2002.

    Google Scholar 

  195. McGrew LL, Takemaru K, Bates R et al. 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; 87(1–2):21–32.

    PubMed  CAS  Google Scholar 

  196. Kazanskaya O, Glinka A, Niehrs C. The role of Xenopus dickkopf1 in prechordal plate specification and neural patterning. Development 2000; 127(22):4981–92.

    PubMed  CAS  Google Scholar 

  197. Kiecker C, Niehrs C. A mornhogen gradient of Wnt/beta-catenin signalling regulates anteroposterior neural patterning in Xenopus. Development 2001; 128(21):4189–201.

    PubMed  CAS  Google Scholar 

  198. Domingos PM, Itasaki N, Jones CM et al. The Wnt/beta-catenin pathway posteriorizes neural tissue in Xenopus by an indirect mechanism requiring FGF signalling. Dev Biol 2001; 239(1):148–60.

    PubMed  CAS  Google Scholar 

  199. Maretto S, Cordenonsi M, Dupont S et al. Mapping Wnt/ta-catenin signaling during mouse development and in colorectal tumors. Proc Natl Acad Sci USA 2003.

    Google Scholar 

  200. Laurent MN, Blitz IL, Hashimoto C et al. The Xenopus homeobox gene twin mediates Wnt induction of goosecoid in establishment of Spemann’s organizer. Development 1997; 124(23):4905–16.

    PubMed  CAS  Google Scholar 

  201. McKendry R, Hsu SC, Harland RM et al. LEF-1/TCF proteins mediate wnt-inducible transcription from the Xenopus nodal-related 3 promoter. Dev Biol 1997; 192(2):420–31.

    PubMed  CAS  Google Scholar 

  202. Vonica A, Gumbiner BM. Zygotic Wnt activity is required for Brachyury expression in the early Xenopus laevis embryo. Dev Biol 2002; 250(1): 112–27.

    PubMed  CAS  Google Scholar 

  203. Arnold SJ, Stappert J, Bauer A et al. Brachyury is a target gene of the Wnt/beta-catenin signaling pathway. Mech Dev 2000; 91(1–2):249–58.

    PubMed  CAS  Google Scholar 

  204. Yang J, Mei W, Otto A et al. Repression through a distal TCF-3 binding site restricts Xenopus myf-5 expression in gastrula mesoderm. Mech Dev 2002; 115(1–2):79–89.

    PubMed  CAS  Google Scholar 

  205. Gradl D, Kuhl M, Wedlich D. The Wnt/Wg signal transducer beta-catenin controls fibronectin expression [In Process Citation]. Mol Cell Biol 1999; 19(8):5576–87.

    PubMed  CAS  Google Scholar 

  206. Vallin J, Thuret R, Giacomello E et al. Cloning and characterization of three Xenopus Slug promoters reveal direct regulation by Lef/ta-catenin signaling. J Biol Chem 2001; 11:11.

    Google Scholar 

  207. Hilton E, Rex M, Old R. VegT activation of the early zygotic gene Xnr5 requires lifting Tcf-mediated repression in the Xenopus blasula. Mech Dev 2003; 120:1127–1138.

    PubMed  CAS  Google Scholar 

  208. Zhang C, Basta T, Hernandez-Lagunas L et al. Repression of nodal expression by maternal B1-type SOXs regulates germ layer formation in Xenopus and zebrafish. Devel Biol 2004; 273:23–37.

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

Copyright information

© 2005 Eurekah.com and Kluwer Academic / Plenum Publishers

About this chapter

Cite this chapter

Klymkowsky, M.W. (2005). Wnt Signaling Networks and Embryonic Patterning. In: Rise and Fall of Epithelial Phenotype. Molecular Biology Intelligence Unit. Springer, Boston, MA. https://doi.org/10.1007/0-387-28671-3_18

Download citation

Publish with us

Policies and ethics