The canonical Wnt pathway in early mammalian embryogenesis and stem cell maintenance/differentiation

Current Opinion in Genetics and Development

Volumn 14, Issue 5, 2004, Pages 533-539

  Wang, Jianbo ^a   Wynshaw Boris, Anthony ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

WNT PROTEIN;

CALCIUM SIGNALING; CELL DIFFERENTIATION; CELL FUNCTION; EMBRYO DEVELOPMENT; GENE CONTROL; GENE FUNCTION; HUMAN; MAMMAL; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; TRANSCRIPTION REGULATION;

ANIMALS; BODY PATTERNING; CELL DIFFERENTIATION; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; SIGNAL TRANSDUCTION; STEM CELLS; TIME FACTORS; WNT PROTEINS;

CNIDARIA; EUKARYOTA; MAMMALIA;

EID: 5444243641     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.gde.2004.07.013     Document Type: Review

References (51)

1. R. Nusse, and H.E. Varmus Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome Cell 31 1982 99 109
2. X. He A Wnt-Wnt situation Dev Cell 4 2003 791 797
3. X. He, M. Semenov, K. Tamai, and X. Zeng LDL receptor-related proteins 5 and 6 in Wnt/beta-catenin signaling: arrows point the way Development 131 2004 1663 1677
4. J.H. van Es, N. Barker, and H. Clevers You Wnt some, you lose some: oncogenes in the Wnt signaling pathway Curr Opin Genet Dev 13 2003 28 33
5. S. Yoshikawa, R.D. McKinnon, M. Kokel, and J.B. Thomas Wnt-mediated axon guidance via the Drosophila Derailed receptor Nature 422 2003 583 588
6. Q. Xu, Y. Wang, A. Dabdoub, P.M. Smallwood, J. Williams, C. Woods, M.W. Kelley, L. Jiang, W. Tasman, and K. Zhang Vascular development in the retina and inner ear: control by Norrin and Frizzled-4, a high-affinity ligand-receptor pair Cell 116 2004 883 895
7. A.H. Wikramanayake, M. Hong, P.N. Lee, K. Pang, C.A. Byrum, J.M. Bince, R. Xu, and M.Q. Martindale An ancient role for nuclear beta-catenin in the evolution of axial polarity and germ layer segregation Nature 426 2003 446 450
8. M.T. Veeman, J.D. Axelrod, and R.T. Moon A second canon. Functions and mechanisms of beta-catenin-independent Wnt signalling Dev Cell 5 2003 367 377
9. W.J. Nelson, and R. Nusse Convergence of Wnt, beta-catenin, and cadherin pathways Science 303 2004 1483 1487
10. D.D. Kaplan, T.E. Meigs, P. Kelly, and P.J. Casey Identification of a role for beta-catenin in the establishment of a bipolar mitotic spindle J Biol Chem 279 2004 10829 10832
11. S.X. Bamji, K. Shimazu, N. Kimes, J. Huelsken, W. Birchmeier, B. Lu, and L.F. Reichardt Role of beta-catenin in synaptic vesicle localization and presynaptic assembly Neuron 40 2003 719 731
12. X. Yu, and R.C. Malenka Beta-catenin is critical for dendritic morphogenesis Nat Neurosci 6 2003 1169 1177
13. N.S. Tolwinski, and E. Wieschaus Rethinking WNT signaling Trends Genet 20 2004 177 181
14. N.S. Tolwinski, M. Wehrli, A. Rives, N. Erdeniz, S. DiNardo, and E Wieschaus Wg/Wnt signal can be transmitted through arrow/LRP5,6 and Axin independently of Zw3/Gsk3β activity Dev Cell 4 2003 407 418 Using two hypomorphic β-catenin alleles, the authors showed that Gsk3β and degradation of β-catenin are dispensable for Wnt signaling. Axin suppresses the transcriptional activation activity of β-catenin in the absence of Gsk3β. Wnt stimulation and activated arrow/Lrp5,6 result in Axin degradation and releasing the transcriptional activation activity of β-catenin.
15. ••], this study showed that in fly, the primary effect of Wnt signaling is to relocalize transgenic Axin-GFP fusion protein to the plasma membrane rather than its degradation. Furthermore, Dishevelled is required in this process. Based on these observations and previous studies, the authors proposed a model that Axin, and presumably the β-catenin destruction complex, are assembled on recycling vesicles. Dishevelled may target these vesicles to the plasma membrane constitutively and Wnt receptors, upon activation, can interact with Axin and retain these vesicles at the plasma membrane to inactivate the destruction complex.
16. F. Cong, and H. Varmus Nuclear-cytoplasmic shuttling of Axin regulates subcellular localization of beta-catenin Proc Natl Acad Sci USA 101 2004 2882 2887
17. K. Takemaru, S. Yamaguchi, Y.S. Lee, Y. Zhang, R.W. Carthew, and R.T. Moon Chibby, a nuclear beta-catenin-associated antagonist of the Wnt/Wingless pathway Nature 422 2003 905 909 The authors identified a conserved nuclear protein Chibby that is an essential inhibitor of the transcriptional activation activity of β-catenin. In cultured mammalian cells, Chibby competes with Lef-1 to bind to β-catenin and suppress β-catenin-mediated transcription. In fly, loss of function of Chibby through RNAi resulted in a Wnt gain-of-function phenotype, indicating an essential role of this protein in antagonizing Wnt activation for normal embryogenesis.
18. K. Tamai, X. Zeng, C. Liu, X. Zhang, Y. Harada, Z. Chang, and X He A mechanism for Wnt coreceptor activation Mol Cell 13 2004 149 156 The authors demonstrated that a reiterated PPPSP motif in the cytoplasmic portion of Lrp5/6/Arrow is both necessary and sufficient, when transferred to the LDL receptor, to activate Wnt signaling. Wnt stimulation causes phosphorylation of the PPPSP motif that may then serve as an inducible docking site for Axin.
19. E. Lee, A. Salic, R. Kruger, R. Heinrich, and M.W. Kirschner The roles of APC and Axin derived from experimental and theoretical analysis of the Wnt pathway PLoS Biol 1 2003 E10 The authors presented a mathematical model for the Wnt pathway based on biochemical experiments using Xenopus eggs. An important observation is that the level of Axin is 5000 times lower than Dsh/Dvl and Apc, and ~2000 times lower than β-catenin and Gsk3β. The very low concentration of Axin may render Wnt signaling to operate with minimal changes in the levels APC and Gsk3β and little perturbation of other pathways. Conversely, they proposed that Apc-dependent Axin degradation may be a critical regulatory mechanism to prevent β-catenin accumulation due to fluctuation of Apc concentration.
20. K.A. Wharton Jr. Runnin' with the Dvl: proteins that associate with Dsh/Dvl and their significance to Wnt signal transduction Dev Biol 253 2003 1 17
21. H.C. Wong, A. Bourdelas, A. Krauss, H.J. Lee, Y. Shao, D. Wu, M. Mlodzik, D.L. Shi, and J. Zheng Direct binding of the PDZ domain of Dishevelled to a conserved internal sequence in the C-terminal region of Frizzled Mol Cell 12 2003 1251 1260
22. C. Kioussi, P. Briata, S.H. Baek, D.W. Rose, N.S. Hamblet, T. Herman, K.A. Ohgi, C. Lin, A. Gleiberman, and J. Wang Identification of a Wnt/Dvl/beta-Catenin → Pitx2 pathway mediating cell-type-specific proliferation during development Cell 111 2002 673 685
23. S.H. Baek, C. Kioussi, P. Briata, D. Wang, H.D. Nguyen, K.A. Ohgi, C.K. Glass, A. Wynshaw-Boris, D.W. Rose, and Rosenfeld MG Regulated subset of G1 growth-control genes in response to derepression by the Wnt pathway Proc Natl Acad Sci USA 100 2003 3245 3250
24. B.J. Thompson A complex of Armadillo, Legless, and Pygopus coactivates dTCF to activate wingless target genes Curr Biol 14 2004 458 466
25. M. Bienz, and H. Clevers Armadillo/beta-catenin signals in the nucleus-proof beyond a reasonable doubt? Nat Cell Biol 5 2003 179 182
26. F. Cong, L. Schweizer, M. Chamorro, and H. Varmus Requirement for a nuclear function of beta-catenin in Wnt signaling Mol Cell Biol 23 2003 8462 8470
27. N.S. Tolwinski, and E. Wieschaus A Nuclear Function for Armadillo/beta-Catenin PLoS Biol 2 2004 E95
28. P. Briata, C. Ilengo, G. Corte, C. Moroni, M.G. Rosenfeld, C.Y. Chen, and R. Gherzi The Wnt/beta-catenin→Pitx2 pathway controls the turnover of Pitx2 and other unstable mRNAs Mol Cell 12 2003 1201 1211
29. T.P. Yamaguchi Heads or tails: Wnts and anterior-posterior patterning Curr Biol 11 2001 R713 R724
30. P. Liu, M. Wakamiya, M.J. Shea, U. Albrecht, R.R. Behringer, and A. Bradley Requirement for Wnt3 in vertebrate axis formation Nat Genet 22 1999 361 365
31. J.C. Hsieh, L. Lee, L. Zhang, S. Wefer, K. Brown, C. DeRossi, M.E. Wines, T. Rosenquist, and B.C. Holdener Mesd encodes an LRP5/6 chaperone essential for specification of mouse embryonic polarity Cell 112 2003 355 367 The authors present phenotypic characterization of a classical mouse mutant, mesoderm development (mesd). Similar to Wnt3 and Lrp5/6 mutants, mesd mutants showed failure in mesoderm and definitive endoderm production, but proper specification of the anterior ectoderm. mesd encodes a protein resides in the endoplasmic reticulum. Studies in cell culture demonstrated conclusively that Mesd could interact with Lrp5 and -6 to prevent intermolecular disulfide-bonded aggregation and retention in the endoplasmic reticulum. Consequently, in collaboration with Receptor-associated protein (Rap), Mesd promotes localization of Lrp5 and 6 to the cell surface.
32. O.G. Kelly, K.I. Pinson, and W.C. Skarnes The Wnt co-receptors Lrp5 and Lrp6 are essential for gastrulation in mice Development 131 2004 2803 2815
33. J. Huelsken, R. Vogel, V. Brinkmann, B. Erdmann, C. Birchmeier, and W. Birchmeier Requirement for beta-catenin in anterior-posterior axis formation in mice J Cell Biol 148 2000 567 578
34. H. Lickert, S. Kutsch, B. Kanzler, Y. Tamai, M.M. Taketo, and R. Kemler Formation of multiple hearts in mice following deletion of beta-catenin in the embryonic endoderm Dev Cell 3 2002 171 181
35. M. Morkel, J. Huelsken, M. Wakamiya, J. Ding, M. van de Wetering, H. Clevers, M.M. Taketo, R.R. Behringer, M.M. Shen, and W. Birchmeier Beta-catenin regulates Cripto- and Wnt3-dependent gene expression programs in mouse axis and mesoderm formation Development 130 2003 6283 6294 Using microarray analysis, the authors found that only a few genes are mis-regulated in the mouse β-catenin mutants despite severe patterning defects. While the expression of some of the known β-catenin target genes such as cyclin D1 and c-Myc are not changed, the expression of Cripto, likely a direct target of β-catenin, is dramatically reduced. In their array analysis, β-catenin mutant embryos also share a common set of mis-regulated genes with Cripto and Wnt3 mutant embryos.
36. T.O. Ishikawa, Y. Tamai, Q. Li, M. Oshima, and M.M. Taketo Requirement for tumor suppressor Apc in the morphogenesis of anterior and ventral mouse embryo Dev Biol 253 2003 230 246
37. I. del Barco Barrantes, G. Davidson, H.J. Grone, H. Westphal, and C. Niehrs Dkk1 and noggin cooperate in mammalian head induction Genes Dev 17 2003 2239 2244
38. J. Huelsken, and W. Birchmeier New aspects of Wnt signaling pathways in higher vertebrates Curr Opin Genet Dev 11 2001 547 553
39. M. Mukhopadhyay, S. Shtrom, C. Rodriguez-Esteban, L. Chen, T. Tsukui, L. Gomer, D.W. Dorward, A. Glinka, A. Grinberg, and S.P. Huang Dickkopf1 is required for embryonic head induction and limb morphogenesis in the mouse Dev Cell 1 2001 423 434
40. U. Nordstrom, T.M. Jessell, and T. Edlund Progressive induction of caudal neural character by graded Wnt signaling Nat Neurosci 5 2002 525 532
41. O.V. Lagutin, C.C. Zhu, D. Kobayashi, J. Topczewski, K. Shimamura, L. Puelles, H.R. Russell, P.J. McKinnon, L. Solnica-Krezel, and G. Oliver Six3 repression of Wnt signaling in the anterior neuroectoderm is essential for vertebrate forebrain development Genes Dev 17 2003 368 379
42. M. Ishibashi, and A.P. McMahon A sonic hedgehog-dependent signaling relay regulates growth of diencephalic and mesencephalic primordia in the early mouse embryo Development 129 2002 4807 4819
43. D. Zechner, Y. Fujita, J. Hulsken, T. Muller, I. Walther, M.M. Taketo, E.B. Crenshaw III, W. Birchmeier, and C. Birchmeier beta-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system Dev Biol 258 2003 406 418
44. H.Y. Lee, M. Kleber, L. Hari, V. Brault, U. Suter, M.M. Taketo, R. Kemler, and L. Sommer Instructive role of Wnt/beta-catenin in sensory fate specification in neural crest stem cells Science 303 2004 1020 1023
45. D. Pinto, A. Gregorieff, H. Begthel, and H. Clevers Canonical Wnt signals are essential for homeostasis of the intestinal epithelium Genes Dev 17 2003 1709 1713
46. M. van de Wetering, E. Sancho, C. Verweij, W. de Lau, I. Oving, A. Hurlstone, K. van der Horn, E. Batlle, D. Coudreuse, and A.P. Haramis The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells Cell 111 2002 241 250
47. E. Sancho, E. Batlle, and H. Clevers Live and let die in the intestinal epithelium Curr Opin Cell Biol 15 2003 763 770
48. C. Jamora, R. DasGupta, P. Kocieniewski, and E. Fuchs Links between signal transduction, transcription and adhesion in epithelial bud development Nature 422 2003 317 322 During hair follicle formation, noggin, a BMP inhibitor, increases Lef1 expression whereas Wnt signaling stablizes β-catenin in skin epithelial stem cells. Unexpectedly, the β-catenin/Lef1 complex functions in hair follicle morphogenesis by repressing E-cadherin expression.
49. K. Willert, J.D. Brown, E. Danenberg, A.W. Duncan, I.L. Weissman, T. Reya, J.R. Yates III, and R. Nusse Wnt proteins are lipid-modified and can act as stem cell growth factors Nature 423 2003 448 452 These authors were the first to purify active Wnt ligands. Notably, whereas purified Wnt3a promotes proliferation and maintenance of the undifferentiated state of haematopoietic stem cell, unpurified Wnt3a-conditioned media induces differentiation of haematopoietic stem cells.
50. T. Reya, A.W. Duncan, L. Ailles, J. Domen, D.C. Scherer, K. Willert, L. Hintz, R. Nusse, and I.L. Weissman A role for Wnt signalling in self-renewal of haematopoietic stem cells Nature 423 2003 409 414 In this study, the authors demonstrated that cultured haematopoietic stem cells (HSC), when infected with a virus expressing constitutively active β-catenin, showed upregulation of HoxB4 and Notch1, remained in an undifferentiated state and proliferate over long period of time. Injection of a small number of the infected HSCs into lethally irradiated mice was sufficient to reconstitute the haematopoietic system in vivo. In contrast, blocking the Wnt pathway in cultured HSCs by interfering with Wnt binding or overexpressing Axin resulted in reduced proliferation and survival rate. The Axin-infected HSCs also show much reduced capacity to reconstitute the haematopoietic system in vivo. This study demonstrated conclusively the essential role of Wnt signaling in HSC self-renewal.
51. A. Polesskaya, P. Seale, and M.A. Rudnicki Wnt signaling induces the myogenic specification of resident CD45+ adult stem cells during muscle regeneration Cell 113 2003 841 852 The authors showed that stem cells expressing the haematopoietic marker CD45 and stem cell antigen-1 (Sca1), when isolated from regenerating muscle, could give rise to myoblasts while those isolated from uninjured muscle can not. Expression of several Wnts and nuclear accumulation of β-catenin were induced in regenerating muscles. Inhibiting Wnt signaling in regenerating muscle blocked myogenic recruitment of CD45+ Sca1+ cells. In contrast, in vitro activation of Wnt signaling could induce myoblast differentiation from CD45+ Sca1+ cells isolated from uninjured muscles.